Towards Sustainable Population Management - Waza
Towards Sustainable Population Management - Waza
Towards Sustainable Population Management - Waza
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Vol 12 2011<br />
<strong>Towards</strong> <strong>Sustainable</strong><br />
<strong>Population</strong> <strong>Management</strong><br />
The Sumatran tiger (Panthera tigris sumatrae) is one of the pioneering taxa for which a Global Species <strong>Management</strong> Plan (GSMP)<br />
has been established under the auspices of WAZA to collaborate inter-regionally on propagating the taxon in human care<br />
and supporting conservation efforts in the wild. | © Harald Löffler
Imprint<br />
Editors:<br />
Markus Gusset & Gerald Dick<br />
WAZA Executive Office<br />
IUCN Conservation Centre<br />
Rue Mauverney 28<br />
CH-1196 Gland<br />
Switzerland<br />
phone: +41 22 999 07 90<br />
fax: +41 22 999 07 91<br />
Layout and typesetting:<br />
michal@sky.cz<br />
Print:<br />
Agentura NP, Staré Město,<br />
Czech Republic<br />
Edition: 750 copies<br />
© WAZA 2011<br />
This edition of WAZA Magazine<br />
is also available on<br />
www.waza.org.<br />
WAZA is a registered<br />
interest representative with<br />
the European Commission,<br />
ID number 30556573017-18.<br />
Printed on FSC paper.<br />
ISSN: 2074-4528<br />
Founding<br />
Member<br />
Contents<br />
Editorial |<br />
Markus Gusset & Gerald Dick ..... 1<br />
Global Programmes for<br />
Sustainability |<br />
Caroline M. Lees &<br />
Jonathan Wilcken .......................2<br />
Maintaining the Status<br />
of Species <strong>Management</strong> in<br />
a Changing Operating<br />
Environment:<br />
Outcomes over Outputs |<br />
Chris Hibbard, Carolyn J. Hogg,<br />
Claire Ford & Amanda<br />
Embury .......................................6<br />
Sustainability of European<br />
Association of Zoos and<br />
Aquaria Bird and Mammal<br />
<strong>Population</strong>s |<br />
Kristin Leus, Laurie Bingaman<br />
Lackey, William van Lint,<br />
Danny de Man, Sanne Riewald,<br />
Anne Veldkam &<br />
Joyce Wijmans .......................... 11<br />
Status of Association of Zoos<br />
and Aquariums Cooperatively<br />
Managed <strong>Population</strong>s |<br />
Sarah Long, Candice Dorsey &<br />
Paul Boyle ................................. 15<br />
Captive <strong>Population</strong>s and<br />
Genetic Sustainability |<br />
Jonathan D. Ballou &<br />
Kathy Traylor-Holzer ................19<br />
Mate Choice as a Potential Tool<br />
to Increase <strong>Population</strong><br />
Sustainability |<br />
Cheryl S. Asa, Kathy<br />
Traylor-Holzer &<br />
Robert C. Lacy .......................... 23<br />
© Nicole Gusset-Burgener<br />
WAZA magazine Vol 12/2011<br />
Zoos Can Lead the Way<br />
with Ex Situ Conservation |<br />
Dalia A. Conde, Nate Flesness,<br />
Fernando Colchero,<br />
Owen R. Jones &<br />
Alexander Scheuerlein .............26<br />
Identifying Gaps and<br />
Opportunities for<br />
Inter-regional Ex Situ<br />
Species <strong>Management</strong> |<br />
Kathy Traylor-Holzer ................30<br />
Which Species Have a Studbook<br />
and How Threatened Are They? |<br />
Frank Oberwemmer,<br />
Laurie Bingaman Lackey &<br />
Markus Gusset .......................... 34<br />
How to Measure Husbandry<br />
Success? The Life Expectancy<br />
of Zoo Ruminants |<br />
Dennis W. H. Müller,<br />
Laurie Bingaman Lackey,<br />
W. Jürgen Streich, Jörns Fickel,<br />
Jean-Michel Hatt &<br />
Marcus Clauss ........................... 37<br />
Intensive <strong>Management</strong><br />
of <strong>Population</strong>s for Conservation |<br />
Anne M. Baker, Robert C. Lacy,<br />
Kristin Leus & Kathy<br />
Traylor-Holzer ...........................40
WAZA magazine Vol 12/2011<br />
Markus Gusset<br />
Editorial<br />
1 & Gerald Dick2 A recent evaluation of the status of<br />
the world’s vertebrates (Hoffmann<br />
et al. 2010; Science 330: 1503–1509)<br />
showed that one-fifth of species are<br />
classified as threatened. On average,<br />
52 species of mammals, birds and<br />
amphibians move closer to extinction<br />
each year. However, the rate of deterioration<br />
would have been at least<br />
one-fifth more in the absence of conservation<br />
measures. Therefore, while<br />
current conservation efforts remain<br />
insufficient to offset the main drivers<br />
of biodiversity loss, this overall pattern<br />
conceals the impact of conservation<br />
successes. Notably, conservation<br />
breeding in zoos and aquariums has<br />
played a role in the recovery of 28%<br />
of the 68 species whose threat status<br />
was reduced.<br />
To fulfil the full suite of conservation<br />
roles required of animal populations<br />
in human care, they must be<br />
demographically robust, genetically<br />
representative of wild counterparts<br />
and able to sustain these characteristics<br />
for the foreseeable future. In<br />
light of growing concerns about the<br />
long-term sustainability of captive<br />
populations, WAZA organised<br />
a two-day workshop in April 2011 on<br />
the sustainable management of zoo<br />
animal populations. This workshop,<br />
which was an integral part of a series<br />
of workshops on related topics<br />
summarised in this edition of the<br />
WAZA Magazine, tackled the issue<br />
of studbook-based global population<br />
management, which lies at the heart<br />
of successful conservation breeding<br />
programmes aimed at preserving<br />
biodiversity.<br />
1 WAZA Conservation Officer &<br />
International Studbook<br />
Coordinator<br />
2 WAZA Executive Director<br />
© Nicole Gusset-Burgener<br />
Lion (Panthera leo) in the Serengeti.<br />
In this edition of the WAZA Magazine,<br />
the results of population sustainability<br />
assessments globally (Lees &<br />
Wilcken) and in three major regions<br />
(Australasia: Hibbard et al.; Europe:<br />
Leus et al.; North America: Long et<br />
al.) are presented. Two important biological<br />
factors impacting population<br />
sustainability are reviewed, namely<br />
genetics (Ballou & Traylor-Holzer) and<br />
mate choice (Asa et al.). Overviews<br />
of how biodiversity is represented in<br />
zoological institutions (Conde et al.),<br />
managed programmes (Traylor-Holzer)<br />
and studbooks (Oberwemmer et<br />
al.) are provided, including a study on<br />
studbook-driven husbandry success<br />
(Müller et al.). Finally, a vision for the<br />
future of population sustainability is<br />
outlined (Baker et al.).<br />
We hope that this edition of the<br />
WAZA Magazine will make a substantial<br />
contribution to the challenge of<br />
how animal populations in human<br />
care can be managed sustainably in<br />
the long term, and thereby further<br />
increase the contribution of the world<br />
zoo and aquarium community to<br />
global biodiversity conservation.<br />
1
2 WAZA magazine Vol 12/2011<br />
Caroline M. Lees<br />
Global Programmes for Sustainability<br />
1 * & Jonathan Wilcken2 Summary<br />
Zoos and aquariums may support<br />
multiple conservation endeavours.<br />
They may be involved in the design<br />
and delivery of environmental education<br />
programmes, support wildlife<br />
research, provide funds, manpower<br />
and expertise in intensive management<br />
to support conservation efforts<br />
and, increasingly, are involved in the<br />
interactive management of captive<br />
and wild populations. These activities<br />
rely on the presence in zoos of living<br />
animal collections. To fulfil all of the<br />
roles required of them, these animal<br />
collections must be demographically<br />
robust, genetically representative of<br />
wild counterparts and able to sustain<br />
these characteristics for the foreseeable<br />
future. Here, we propose a definition<br />
of a “sustainable” population, describe<br />
the challenges in building one<br />
and explore the potential of global<br />
species management programmes to<br />
overcome some of these challenges.<br />
1 IUCN/SSC Conservation Breeding<br />
Specialist Group Australasia,<br />
c/o Auckland Zoo, Auckland,<br />
New Zealand<br />
2 Auckland Zoo, Auckland, New Zealand<br />
* E-mail for correspondence:<br />
caroline@cbsgaustralasia.org<br />
<strong>Sustainable</strong><br />
<strong>Population</strong>s<br />
We define a sustainable population<br />
here as one that is able to persist,<br />
indefinitely, with the resources<br />
available to it. Under this definition,<br />
sustainable populations fall into two<br />
categories:<br />
Category 1: Self-sustaining <strong>Population</strong>s.<br />
This includes populations with<br />
sufficient internal resources to persist<br />
without supplementation. That is,<br />
they are large enough to withstand<br />
or avoid the otherwise damaging<br />
effects of small population size (i.e.<br />
naturally fluctuating birth and death<br />
rates, sex ratio skews, inbreeding,<br />
low gene diversity) (Frankham et al.<br />
2002). <strong>Population</strong>s in this category<br />
are necessarily very large.<br />
Category 2: Supplemented <strong>Population</strong>s.<br />
This second category contains populations<br />
that, usually because of their<br />
smaller size, do not have sufficient internal<br />
resources for self-sustainability,<br />
but are supported by external supplementation.<br />
For the sustainability test<br />
to be satisfied, this supplementation<br />
must be from source populations able<br />
themselves to sustain the required<br />
harvest without depletion. A population<br />
of any size can be sustainable<br />
provided that the supplementing<br />
source population can accommodate<br />
the required harvest. The larger and<br />
better managed the population, the<br />
lower the rate of supplementation<br />
needed.<br />
Fig. 1<br />
Recommended allocation of captive resources<br />
based on IUCN categories of extinction risk<br />
(modified from Lees & Wilcken 2009).<br />
It seems reasonable to suggest that<br />
all taxa for which the captive population<br />
constitutes a significant part of<br />
the species’ genome, or for which<br />
further collection from the wild is<br />
considered impossible, should be<br />
managed as self-sustaining captive<br />
populations. Included would be all<br />
species categorised by the International<br />
Union for Conservation of<br />
Nature (IUCN) as Extinct in the Wild<br />
or Critically Endangered, and some of<br />
those categorised as Endangered or<br />
Vulnerable.<br />
On the other hand, those species<br />
for which further collection from the<br />
wild is still considered a viable and<br />
responsible option may be more efficiently<br />
maintained through periodic,<br />
minimal and scientifically calculated<br />
rates of supplementation from the<br />
wild (Fig. 1). It is important that population<br />
size targets are calculated and<br />
periodically revised for each individual<br />
population, based on its characteristics<br />
and management. However,<br />
indicative ranges of population sizes<br />
can be suggested for each of these<br />
categories of sustainability.
WAZA magazine Vol 12/2011<br />
Targets for<br />
Self-sustainability<br />
For self-sustainability, populations<br />
ought to encounter no net loss of<br />
genetic diversity. Genetic diversity<br />
is the raw material for evolution<br />
and as it declines so does a population’s<br />
adaptive potential (Frankham<br />
et al. 2002). Genetic diversity is<br />
lost through non-random breeding<br />
and chance processes (drift), and is<br />
gained by mutation. The smallest<br />
population size for which drift is balanced<br />
by mutation is estimated to be<br />
about N e = 500 (Frankham et al. 2002),<br />
where N e is the effective population<br />
size and genetic diversity is measured<br />
through heterozygosity and additive<br />
genetic variance. N e is a measure of<br />
that proportion of the census population<br />
that is contributing to the next<br />
generation.<br />
The ratio of effective to actual population<br />
size (N e /N) is greatest where<br />
the number of animals that reproduce<br />
is high, the sex ratio of breeding<br />
animals is equal and the life-time<br />
family sizes of reproducing animals<br />
are also equal, with the latter having<br />
most influence in zoo populations.<br />
Wild populations differ significantly<br />
from these ideal characteristics and<br />
may achieve N e /N ratios of around 0.1<br />
(Frankham et al. 2002). That is, they<br />
may require about 5,000 animals<br />
to achieve a sustainable effective<br />
population size of 500. Through management,<br />
captive populations can be<br />
brought closer to these ideal characteristics,<br />
regularly showing N e /N ratios<br />
of 0.2–0.4, though ratios as high<br />
as 0.7 have been reported (Willis &<br />
Wiese 1993). Based on these reported<br />
ratios, for captive populations to be<br />
self-sustaining, they will need an N e<br />
of at least 500, or an actual population<br />
size of 700–1,900 animals.<br />
Targets for<br />
Supplemented<br />
Sustainability<br />
Models suggest that it is possible to<br />
retain relatively high levels of gene<br />
diversity in population sizes smaller<br />
than N e = 500 if coupled with periodic<br />
addition of new founders (Lacy 1987;<br />
Willis & Wiese 1993). At low population<br />
sizes (50–100), the supplementation<br />
rates required are too high to be<br />
contemplated (Willis & Wiese 1993)<br />
and demographic factors pose a real<br />
risk. However, at an N e of 120, Lacy<br />
(1987) calculated that it is possible<br />
to retain 95% of wild gene diversity<br />
with the addition of five new founders<br />
each generation. In zoos, N e = 120<br />
could equate to somewhere between<br />
170 and 460 animals, depending on<br />
the effectiveness of management.<br />
It should be noted that the extent<br />
to which new wild founders may be<br />
responsibly available will depend on<br />
political and community sensitivities,<br />
and logistical and biological constraints.<br />
Any such initiatives should<br />
be based on an appropriate assessment<br />
of wild population viability.<br />
Global Potential<br />
In addition to sufficient size, populations<br />
need to be imbued with enough<br />
gene diversity in the form of founders,<br />
and they need to sustain the<br />
requisite growth rate to avoid large<br />
fluctuations in size. In recent years,<br />
a number of studies, including the<br />
one on which this article is based<br />
(Lees & Wilcken 2009), have shown<br />
that regional population management<br />
programmes are not achieving<br />
the conditions for sustainability. They<br />
are too small, are based on too few<br />
founders and are not achieving the<br />
required growth rates.<br />
Global Sustainability<br />
However, a review of potential across<br />
regions suggests that a move to<br />
global coordination would overcome<br />
some of the current within-region<br />
limitations. For example, of the populations<br />
registered in international<br />
studbooks (ISIS/WAZA 2005), 57.3%<br />
fall within the population size range<br />
required for supplemented sustainability,<br />
as it is described above.<br />
In addition to species registered in<br />
international studbooks and again<br />
using data from the International<br />
Species Information System (ISIS), we<br />
estimate that by linking up regionally<br />
managed populations into global programmes,<br />
the average population size<br />
for vertebrate taxa can be increased<br />
from 120 to 170, placing many more<br />
taxa within the accessible range for<br />
supplemented sustainability.<br />
Further, of the populations registered<br />
in international studbooks (ISIS/<br />
WAZA 2005), 9% fall within the population<br />
size range for self-sustainability,<br />
including scimitar-horned oryx (Oryx<br />
dammah) (Extinct in the Wild), Przewalski’s<br />
horse (Equus ferus przewalskii)<br />
(Critically Endangered) and Amur<br />
tiger (Panthera tigris altaica) (Endangered)<br />
– all of which fall into risk<br />
categories where self-sustainability is<br />
either advisable or essential (Fig. 2).<br />
3<br />
»
»<br />
4 Global Sustainability<br />
WAZA magazine Vol 12/2011<br />
Global versus Regional<br />
<strong>Management</strong><br />
Despite the obvious sustainability<br />
advantages of global management, it<br />
remains the exception and regional<br />
management the norm. The reasons<br />
for this are easily identified: within-<br />
region transfers are logistically<br />
simpler and often less expensive, permitting<br />
and quarantine requirements<br />
are less onerous and the necessary<br />
administrative structures and lines of<br />
communication are (usually) better<br />
established and more effective. Indeed,<br />
the zoo region is often the most<br />
sensible unit for cooperation, particularly<br />
for local species that are the<br />
focus of short-term breed-for-release<br />
initiatives. However, as described<br />
above, many regional populations are<br />
not reaching viable sizes. <strong>Population</strong>s<br />
tracked across multiple regions reach<br />
necessarily larger sizes. Inter-regional<br />
or global management, though<br />
difficult to implement successfully,<br />
offers not only the advantage of scale<br />
but also of strategic overview. For<br />
example:<br />
• For small, widely dispersed populations,<br />
global management provides<br />
an opportunity to link up a number<br />
of isolated, unsustainable units,<br />
improving demographic stability<br />
and managing inbreeding and gene<br />
diversity more effectively.<br />
• Research demonstrates that the<br />
genetic diversity of large global<br />
populations may benefit from<br />
strategic population subdivision and<br />
restricted but carefully managed<br />
migration between these subpopulations.<br />
Regional populations offer<br />
convenient subpopulations for use<br />
in this context.<br />
• For expanding populations that are<br />
primarily held in one region but<br />
sought after in others, global management<br />
may be a useful mechanism<br />
for distributing important<br />
founder lines so that overall genetic<br />
diversity is maximised. In the ab-<br />
Fig. 2<br />
Przewalski’s horses are potentially<br />
self-sustaining at a global level.<br />
© Chris Walzer/International Takhi Group<br />
sence of such management, overrepresented<br />
lines are often continually<br />
exported from the source region<br />
to found new populations. This can<br />
reduce the genetic potential and<br />
therefore the conservation value<br />
of those populations and of overall<br />
global stocks.<br />
In certain circumstances then, global<br />
management offers greater potential<br />
for extending the viability of zoo<br />
populations and improving their<br />
value to conservation. For this potential<br />
to be reached, global management<br />
needs to be a more accessible<br />
option. The new WAZA framework for<br />
Global Species <strong>Management</strong> Plans<br />
(GSMPs) provides this access and its<br />
use should be encouraged.
WAZA magazine Vol 12/2011<br />
Recommendations<br />
If zoo populations are not sustainable,<br />
neither are zoos themselves. Too few<br />
populations are currently satisfying<br />
the conditions for sustainability.<br />
There is scope for reversing this trend<br />
but it requires renewed commitment<br />
and new investment. The following<br />
five-point plan summarises steps that<br />
could be taken towards this end.<br />
Step 1: Global Audit. A complete audit<br />
of WAZA populations to provide<br />
a useful snapshot of potential, for use<br />
in planning.<br />
Step 2: Global Planning. An inclusive<br />
process, based on the audit, to identify<br />
a list of priority species for global<br />
management, based on population<br />
potential as well as wild status.<br />
Step 3: Global Targets. Calculation<br />
of global target population sizes for<br />
each priority species, based on appropriate<br />
science and a rationale of<br />
sustainability:<br />
• All taxa categorised by IUCN as Extinct<br />
in the Wild or Critically Endangered<br />
should be assigned a target<br />
N e of 500 (700 < N < 1,900).<br />
• All other taxa for which recruitment<br />
from the wild is considered inappropriate<br />
or impossible should also be<br />
assigned a target N e of 500.<br />
• For taxa where recruiting new<br />
founders is not considered inappropriate<br />
or impossible, an N e of<br />
120 (170 < N < 460) should be the<br />
target, in conjunction with the input<br />
of around five new founders each<br />
generation.<br />
• Exceptions to this could be: taxa<br />
being deliberately phased out, taxa<br />
present for short-term research or<br />
breed-for-release programmes and<br />
taxa for which there are established<br />
gene banks that allow gene<br />
diversity targets to be met at lower<br />
numbers (noting that demographic<br />
considerations should dictate the<br />
minimum number in such cases).<br />
Step 4: Global Investment. Appropriate<br />
investment in professional species<br />
managers, husbandry innovation<br />
and supporting technology. This<br />
will help ensure that science-based<br />
targets are set and that programmes<br />
are designed and managed to meet<br />
those targets at achievable population<br />
sizes.<br />
Step 5: Global Commitment.<br />
Long-term programmes require<br />
long-term commitment. Mechanisms<br />
for securing this commitment from<br />
participating zoos should be factored<br />
into industry benchmarking and accreditation<br />
programmes.<br />
Sustaining the viability and genetic<br />
value of zoo populations requires<br />
larger, better founded and more<br />
imaginatively managed populations<br />
than we often have at our disposal.<br />
A concerted move away from<br />
regional and towards global coordination<br />
of genetic and demographic<br />
management has the potential to<br />
dramatically improve the quality of<br />
captive resources available to support<br />
wild populations of many species.<br />
Fully mobilising that resource will be<br />
challenging, but must be a priority<br />
for the world’s zoos over the coming<br />
decade.<br />
References<br />
Global Sustainability 5<br />
• Frankham, R., Ballou, J. D. &<br />
Briscoe, D. A. (2002) Introduction<br />
to Conservation Genetics. Cambridge:<br />
Cambridge University<br />
Press.<br />
• ISIS/WAZA (2005) Studbook Library<br />
CD-ROM. Eagan, MN: ISIS.<br />
• Lacy, R. C. (1987) Loss of genetic<br />
diversity from managed populations:<br />
interacting effects of drift,<br />
mutation, immigration, selection,<br />
and population subdivision. Conservation<br />
Biology 1: 143–158.<br />
• Lees, C. M. & Wilcken, J. (2009)<br />
Sustaining the Ark: the challenges<br />
faced by zoos in maintaining<br />
viable populations. International<br />
Zoo Yearbook 43: 6–18.<br />
• Willis, K. & Wiese, R. J. (1993)<br />
Effect of new founders on retention<br />
of gene diversity in captive<br />
populations: a formalization of<br />
the nucleus population concept.<br />
Zoo Biology 12: 535–548.
6 WAZA magazine Vol 12/2011<br />
Chris Hibbard<br />
Maintaining the Status of Species<br />
<strong>Management</strong> in a Changing Operating<br />
Environment: Outcomes over Outputs<br />
1 *, Carolyn J. Hogg1 , Claire Ford1 & Amanda Embury2 Summary<br />
The Australasian region’s Zoo and<br />
Aquarium Association (ZAA) is recognised<br />
internationally for its innovative<br />
approach to species management.<br />
A 2005 review of species management<br />
in the region highlighted an<br />
alarming proportion of species that<br />
were unlikely to be sustainable in<br />
the long term. In reaction to this, the<br />
Australasian Species <strong>Management</strong><br />
Program (ASMP) developed a benchmarking<br />
tool, the ASMP Health<br />
Check Report, to measure fact-based<br />
criteria by breaking down species<br />
management into measurable components.<br />
The Health Check Report<br />
is structured into four portfolios:<br />
Administration, Science, Legislation<br />
and Overall Performance. The results<br />
of the Health Check Report allow<br />
ZAA to monitor the performance of<br />
ASMPs and better understand the<br />
1 Zoo and Aquarium Association<br />
Australasia, Sydney, Australia<br />
2 Australasian Species <strong>Management</strong><br />
Program, c/o Zoos Victoria,<br />
Melbourne, Australia<br />
* E-mail for correspondence:<br />
chris@zooaquarium.org.au<br />
skills/expertise required to deliver the<br />
desired outcomes. Results are also<br />
incorporated into any annual report<br />
that is provided to directors of member<br />
organisations to provide succinct<br />
advice about the performance of<br />
ASMPs to which they contribute. The<br />
Health Check Report allows for an<br />
up-to-date assessment of managed<br />
programmes within their scope and<br />
activities, while providing assurance<br />
to the ZAA Board of Directors, and<br />
ultimately the membership, on the<br />
improvement, accountability and<br />
persistence of the region’s priority<br />
programmes.<br />
Introduction<br />
The Australasian zoo and aquarium<br />
environment is geographically isolated,<br />
relatively small in population<br />
size and has a rigorous legislative<br />
environment. As a result, it has an<br />
established regional commitment to<br />
cooperative species management,<br />
a particular necessity with exotic<br />
species. As the conditions of geography,<br />
population and legislation are<br />
non-abating, it is vital that the region<br />
not only remains at the forefront of<br />
species management but recognises<br />
the importance of ongoing review<br />
and assessment of our species management<br />
performance. Small population<br />
biology in support of species<br />
management has been utilised by<br />
the zoo industry since the mid-1990s<br />
(reviewed in Ballou et al. 2010), and<br />
more recently the importance of sustainability<br />
relative to the challenges<br />
faced by zoos in maintaining viable<br />
populations has been discussed (Lees<br />
& Wilcken 2009). Of specific relevance<br />
to this article is the issue raised by<br />
Lees & Wilcken (2009) over implementing<br />
recommendations within<br />
institutions.
WAZA magazine Vol 12/2011<br />
In 2008, the Australasian Species<br />
<strong>Management</strong> Program (ASMP),<br />
the species management arm of<br />
ZAA, commissioned a review of the<br />
delivery of species management outcomes<br />
within the Australasian region.<br />
The initial discussion related largely<br />
to exotic taxa and was prefaced by<br />
a report prepared on the status of all<br />
exotic taxa under formal management<br />
within the Australasian region.<br />
The report suggested that an alarming<br />
proportion of exotic taxa were<br />
unlikely to be sustainable in the long<br />
term, including some which were<br />
facing imminent local extinctions in<br />
Australasian zoos (Barlow & Hibbard<br />
2005). The scope of this discussion<br />
quickly expanded to include all Australasian<br />
programmes (both native<br />
and exotic) where a level of formal<br />
management had been applied.<br />
The ASMP Committee, through the<br />
ZAA Board of Directors, launched<br />
a full review of species management<br />
services under the banner of the<br />
Future Directions Project. The ASMP<br />
Committee recognised the sound<br />
foundations already in place and focused<br />
on addressing issues that had<br />
arisen as a result of the programme<br />
maturing and operating environments<br />
evolving. In broad terms, the<br />
project was to examine resourcing,<br />
policies, processes and species to be<br />
managed. In order to apply specific<br />
and measured resolutions, the<br />
project was tasked with determining<br />
the specific causes for the shortfall in<br />
overall population “health” of species<br />
in managed programmes and establishing<br />
actions to resolve these.<br />
The aim of the project was to improve<br />
the effectiveness of species management<br />
programmes through accountability,<br />
disciplined processes and<br />
inclusiveness, in order for the ASMP<br />
to remain current and relevant as<br />
a member service to the ZAA membership.<br />
Methodology<br />
The ASMP Future Directions Project<br />
commenced in 2008 and was earmarked<br />
for completion in 2010. There<br />
were various components to the project<br />
beginning with a rigorous review<br />
of the species selected for management<br />
and the level to which they could<br />
or should be managed. This article will<br />
not attempt to document the species<br />
review process, other than to recognise<br />
that many excellent models have<br />
been developed and that the Australasian<br />
model was not radically different<br />
from others in current use; that is, it<br />
addresses key goals identified in the<br />
World Zoo and Aquarium Conservation<br />
Strategy (WAZA 2005). For exotic<br />
taxa, the Australasian model rated<br />
highly the ongoing ability to acquire<br />
the species both in terms of import<br />
legislation and access to new genetic<br />
material (either by inter-regional or<br />
range state sources). This was of specific<br />
importance given the small size<br />
of our regional populations and the<br />
need to rely on periodic importation to<br />
sustain most populations.<br />
The next step in the process was the<br />
development of a benchmarking<br />
tool with the current working title of<br />
the ASMP Health Check Report. The<br />
Health Check Report is by no means<br />
a completed piece of work and continues<br />
to evolve to reflect a changing<br />
zoo environment and respond to<br />
any issues that might be identified in<br />
the future. In the past, ZAA has used<br />
a compliance report to measure institutional<br />
adherence to specific recommendations<br />
on specimen transfers<br />
and breeding based on studbook<br />
analysis. The development of the<br />
Health Check Report has expanded<br />
the scope substantially and shifts the<br />
focus of assessment onto the delivery<br />
of a suite of measurable programme<br />
goals rather than the performance of<br />
individual contributors. The Health<br />
Check Report measures the overall<br />
health of the programme as well as<br />
giving insight into the “health” of<br />
specific areas.<br />
ZAA Sustainability<br />
It was acknowledged that in many<br />
cases sound scientific principles of<br />
small population biology had been<br />
applied; however, the results in<br />
programme performance were not<br />
all meeting expectations. A number<br />
of claims were put forward, many<br />
of which were consistent with those<br />
identified by Lees & Wilcken (2009),<br />
and included:<br />
• A lack of spaces being offered for<br />
managed species, fuelled by a trend<br />
away from multiple, small, speciesspecific<br />
facilities to larger multi-taxa<br />
“experiences”, including a move<br />
away from extensive off-display<br />
holding facilities.<br />
• Government legislation over the<br />
import of exotic taxa was having<br />
a negative impact on founder recruitment<br />
for populations.<br />
• Species biology in some instances<br />
was not necessarily aligned with the<br />
mean kinship and genetic management<br />
employed.<br />
• The concept that genetic management<br />
was better understood and<br />
more rigorously applied by species<br />
coordinators than demographic<br />
management and in some instances<br />
contributed to demographic instability.<br />
• Species management expertise and<br />
innovation required further development.<br />
• Implementation of specific programme<br />
recommendations although<br />
usually attempted often was<br />
not necessarily achieved, or resulted<br />
in the desired outcome.<br />
The Health Check Report was developed<br />
to measure fact-based criteria,<br />
by breaking down species management<br />
practices into measurable components.<br />
This enables a programme’s<br />
performance to be quickly assessed<br />
and any remedial measures applied in<br />
a timely manner where programmes<br />
are seen to be falling short of expectation.<br />
In addition, it allows for the acknowledgement<br />
of positive progress<br />
and feedback to the many species<br />
coordinators hosted by member zoos.<br />
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8 ZAA Sustainability<br />
WAZA magazine Vol 12/2011<br />
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The Health Check Report considers<br />
four broad portfolios with associated<br />
responsibilities and criteria for<br />
programme performance, as set<br />
out in Table 1. Each criterion has<br />
predetermined scoring parameters<br />
that is then translated into a traffic<br />
light system of green (performing<br />
well), orange (needs some specific<br />
attention) and red (needs immediate<br />
attention). The parameters for<br />
each criterion were set necessarily<br />
high to ensure the report represents<br />
a true level of current achievement.<br />
The scoring does not try to suggest<br />
a long-term level of sustainability,<br />
but attempts to isolate some issues<br />
around immediate need and priority<br />
for resource allocation.<br />
Previously used species management<br />
criteria, such as purpose, role or<br />
threat status, were no longer considered,<br />
as these are assessed as part of<br />
the initial species selection process.<br />
The Health Check Report is designed<br />
to look specifically at the operational<br />
and sustainability performance of the<br />
species management programme<br />
after species selection and identification<br />
of what conservation contribution<br />
or purpose the population fulfils.<br />
As an example of the benefits of the<br />
Health Check Report, only the results<br />
for the exotic fauna programmes are<br />
presented here for discussion. The<br />
data relate to 40 intensively managed<br />
exotic species programmes in<br />
the order Mammalia. No exotic bird<br />
programmes are managed by ZAA<br />
due to the significant restrictions<br />
on the importation of birds to the<br />
region since the 1950s, and the small<br />
numbers of exotic reptiles that are<br />
managed are grouped with the native<br />
reptile data.<br />
Table 1.<br />
ASMP Health Check Report: portfolios, responsibilities and scoring criteria.<br />
Portfolio Primary responsibility Examples of scored criteria<br />
Administration ZAA ASMP staff Species coordinator assigned, studbook currency<br />
and accuracy, annual report tendered<br />
(and currency), level of assistance provided<br />
to species coordinator, Captive <strong>Management</strong><br />
Plan developed, etc.<br />
Science Species coordinators, Taxon<br />
Advisory Groups and participating<br />
institutions (with<br />
assistance from the ASMP for<br />
specific small population biology<br />
issues as required)<br />
Retained genetic diversity, average inbreeding,<br />
success of recommended transfers and<br />
breeding, etc.<br />
Legislation ASMP Committee Status of legislation in regard to the import<br />
from a variety of sources (including range<br />
states). Restrictions on the keeping of species<br />
within the region (based on pest potential,<br />
etc.). This set of criteria is individually tailored<br />
to exotic, Australian native and New Zealand<br />
native fauna.<br />
Overall<br />
Performance<br />
ZAA Board of Directors The overall performance score is an amalgamated<br />
performance of all three criteria<br />
above. Specific attention is focused on any<br />
programme with an overall red score.<br />
Results and Discussion<br />
Administration. There is a demonstrated<br />
high compliance of the<br />
administration of the ASMPs (Fig. 1),<br />
with almost all programmes having<br />
a species coordinator assigned; the<br />
required reporting and interpretation<br />
of studbook data using PM2000<br />
(Annual Report and Recommendation<br />
submitted) being tendered with<br />
relatively moderate coaching by the<br />
senior species management staff in<br />
the ZAA office (species coordinator<br />
assistance); and the facilities<br />
nominated score refers to adequate<br />
spaces dedicated to the programme<br />
(50 spaces), as set out in the ASMP<br />
Regional Census and Plan. The significant<br />
challenge for the region is the<br />
need to further develop a number of<br />
strategic planning documents in the<br />
form of Captive <strong>Management</strong> Plans<br />
(CMPs).<br />
Science. The portfolio with the<br />
greatest proportion of factors in the<br />
red zone, and so requiring immediate<br />
attention, are those found in<br />
the Science portfolio (Fig. 1). It is<br />
thought that several factors may be<br />
cumulating within this area, where<br />
the transfer failure impacts on the<br />
planned breeding, which in turn may<br />
affect the scores for genetic diversity<br />
(scored as retained at 90% or higher),<br />
inbreeding (average for population is<br />
lower than 0.125) and mean kinship<br />
(average for population is lower than<br />
0.125). Despite some obvious issues<br />
with breeding to plan in addition to<br />
transfer failure, population trends<br />
remain positive. Further investigation<br />
is required to determine which proportion<br />
of the population trend is as<br />
a result of importation over breeding.
WAZA magazine Vol 12/2011<br />
Fig. 1<br />
ASMP Health Check Report: percentage of scoring in each of three major portfolios and overall<br />
across 40 intensively managed exotic mammals in ZAA membership, where green (performing<br />
well), orange (needs some specific attention) and red (needs immediate attention).<br />
Legislation. The results of the Legislation<br />
portfolio have been useful in that<br />
legislative barriers have long been<br />
considered the significant cause for<br />
shortfall in programme performance<br />
(Fig. 1). It is clearly demonstrated that<br />
there is an ability to import a majority<br />
of the targeted exotic species<br />
into the region, and that interaction<br />
between New Zealand and Australia<br />
is also well supported by legislation<br />
(vital for effective Australasian-based<br />
programmes). There is a requirement<br />
from the Australian government<br />
for all species listed in Appendix I of<br />
the Convention on International<br />
Trade in Endangered Species of Wild<br />
Fauna and Flora (CITES) to have an<br />
approved Cooperative Conservation<br />
Plan in place prior to any international<br />
transaction and these are<br />
largely covered in regard to current<br />
need. As with other regions, the access<br />
to new founders is a challenge<br />
for a large number of programme<br />
species. The VPC threat category is<br />
a rating applied by the Australian<br />
government on the pest potential of<br />
a species to the environment (including<br />
public safety), if it were to escape<br />
and establish. The results here assist<br />
in identifying the promotion of appropriate<br />
biosecurity measures in our<br />
member zoos, which in turn provides<br />
confidence in granting permits to<br />
hold such species.<br />
Overall Performance. The overall<br />
performance scores (Fig. 1) show<br />
approximately 75% of all the exotic<br />
programmes within the sample either<br />
in good order (green) or with some<br />
specific issues (yellow).<br />
Conclusions<br />
ZAA Sustainability<br />
The Health Check Report process has<br />
allowed ZAA to commence a measured<br />
approach to the assessment<br />
of its intensively managed species<br />
programme performance. It is by no<br />
means exhaustive but does represent<br />
an ongoing commitment to self-assessment<br />
and a structured approach<br />
to problem solving, communicating<br />
priorities and deployment of resources.<br />
This will provide tangible benefits<br />
to supporting programme goals and<br />
assurances and value to the membership<br />
of ZAA who jointly fund the<br />
association’s activities.<br />
The process has allowed us to mobilise<br />
resources into the areas of most<br />
need. Recently the results have been<br />
fed into the region’s Taxon Advisory<br />
Group (TAG) structure, with each TAG<br />
charged with developing a specific<br />
action plan against any species with<br />
a red score. As a consequence, there<br />
has been support in aligning the<br />
actions of the TAGs, with a greater focus<br />
on animal husbandry and behaviour<br />
along with the identification of<br />
staff training and development. It is<br />
hoped that this will have a direct and<br />
positive impact in the areas of animal<br />
transfers and breeding.<br />
The legislative assessment has<br />
proven to be very productive, as it<br />
has long been considered throughout<br />
the membership as a primary<br />
limitation to programme progress.<br />
Although hoofstock imports continue<br />
to provide biosecurity challenges<br />
for the region due to the existing<br />
commercial livestock industry in both<br />
New Zealand and Australia, a majority<br />
of the other taxa can be imported<br />
under current legislation.<br />
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10 ZAA Sustainability<br />
WAZA magazine Vol 12/2011<br />
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Of significant interest were the findings<br />
of the Health Check Report that<br />
highlighted the challenges associated<br />
with achieving recommended<br />
animal transfers and breeding.<br />
There is a need for detailed assessment<br />
of contributing factors so that<br />
resolutions can be developed. These<br />
outcomes may also indicate a need<br />
for greater alignment of genetic<br />
management strategies with the biology<br />
of the species in order to support<br />
long-term sustainability outcomes.<br />
In addition to providing direct<br />
feedback into the TAGs, the results<br />
of the Health Check Report now<br />
feature in every executive summary<br />
for all Annual Reports and Recommendations<br />
generated for intensively<br />
managed populations. The executive<br />
summary also includes graphical<br />
evidence of the five-year trends of<br />
both the genetic and demographic<br />
management of the programme, as<br />
well as reporting against the strategic<br />
goals of the CMP (where these have<br />
been developed), or against a set of<br />
generic managed programme goals.<br />
These executive summaries will be<br />
collated at the end of every year and<br />
published as a Director’s Executive<br />
Summary, so programme performance<br />
is not only being reported to<br />
curators and keepers, but also to the<br />
chief executive officers and directors,<br />
allowing all those involved to gain<br />
an understanding of how the programme<br />
is tracking both in the short<br />
and long term.<br />
As described, the Health Check Report<br />
is not a complete piece of work<br />
but rather an evolving one. Although<br />
there appears to be a good delivery<br />
on annual reporting by species coordinators,<br />
in the future ZAA will be<br />
devoting a concerted effort towards<br />
the development of a greater suite<br />
of CMPs that guide a more strategic<br />
approach over the longer term. To<br />
date ZAA has already completed the<br />
realignment of the CMP process to<br />
meet a range of operational, small<br />
population biology and business<br />
outcomes.<br />
In conclusion, the Health Check<br />
Report:<br />
• currently provides every TAG with<br />
an up-to-date assessment of the<br />
managed programmes within their<br />
scope and focuses activities on<br />
constant improvement;<br />
• allows the ASMP Committee to ensure<br />
that all managed programmes<br />
are receiving the appropriate level<br />
of attention from the TAGs, participating<br />
institutions and ZAA species<br />
management staff;<br />
• provides the membership of ZAA<br />
and its Board of Directors an assurance<br />
that a detailed level of scrutiny<br />
will ensure every effort is applied to<br />
continued improvement, accountability<br />
and persistence of the region’s<br />
priority populations.<br />
The Health Check Report provides<br />
a succinct graphic representation of<br />
the performance of our managed<br />
species programmes, clearly capturing<br />
the outcomes towards agreed<br />
goals achieved during the year.<br />
Acknowledgements<br />
We are grateful to Stephanie Behrens<br />
from the ZAA New Zealand Office for<br />
helpful feedback on this article and<br />
the ASMP Committee for their continued<br />
support and encouragement<br />
of this project.<br />
References<br />
• Ballou, J. D., Lees, C., Faust, L. J.,<br />
Long, S., Lynch, C., Bingaman<br />
Lackey, L. & Foose, T. J. (2010)<br />
Demographic and genetic management<br />
of captive populations.<br />
In: Wild Mammals in Captivity:<br />
Principles and Techniques for Zoo<br />
<strong>Management</strong>, 2nd ed. (ed. by<br />
Kleiman, D. G., Thompson, K.<br />
V. & Kirk Baer, C.), pp. 219–252.<br />
Chicago, IL: University of Chicago<br />
Press.<br />
• Barlow, S. C. & Hibbard, C. (2005)<br />
Going, going, gone. A zoo without<br />
exotic mammals? ARAZPA Submission<br />
148b. Canberra: Department<br />
of Agriculture, Fisheries<br />
and Forestry.<br />
• Lees, C. M. & Wilcken, J. (2009)<br />
Sustaining the Ark: the challenges<br />
faced by zoos in maintaining<br />
viable populations. International<br />
Zoo Yearbook 43: 6–18.<br />
• WAZA (2005) Building a Future<br />
for Wildlife: The World Zoo and<br />
Aquarium Conservation Strategy.<br />
Berne: WAZA.
WAZA magazine Vol 12/2011 11<br />
Kristin Leus 1,2 *, Laurie Bingaman Lackey 3 , William van Lint 1 ,<br />
Danny de Man 1 , Sanne Riewald 4 , Anne Veldkam 4 & Joyce Wijmans 4<br />
Sustainability of European<br />
Association of Zoos and Aquaria<br />
Bird and Mammal <strong>Population</strong>s<br />
Introduction<br />
A rapid assessment of the sustainability<br />
of bird and mammal populations<br />
managed by the European Association<br />
of Zoos and Aquaria (EAZA) as<br />
European Endangered Species Programmes<br />
(EEPs) and European Studbooks<br />
(ESBs) was initiated in 2008, in<br />
response to concerns arising from the<br />
European Union (EU) bird import ban<br />
triggered by avian influenza. There is<br />
as yet no such blanket ban for mammal<br />
populations, but we have already<br />
experienced transport restrictions<br />
for various groups of mammals in<br />
response to disease outbreaks, such<br />
as bluetongue, bovine spongiform<br />
encephalopathy (BSE) and foot-andmouth.<br />
All of this begs the questions<br />
“are, or can, EAZA bird and mammal<br />
populations be sustainable” and<br />
“what do we mean by sustainable”?<br />
1 European Association of Zoos<br />
and Aquaria, Amsterdam,<br />
The Netherlands<br />
2 IUCN/SSC Conservation Breeding<br />
Specialist Group Europe,<br />
c/o Copenhagen Zoo,<br />
p/a Merksem, Belgium<br />
3 International Species Information<br />
System, Eagan, MN, USA<br />
4 Van Hall Larenstein University<br />
of Applied Sciences, Leeuwarden,<br />
The Netherlands<br />
* E-mail for correspondence:<br />
kristin@cbsgeurope.eu<br />
Self-sustainability generally implies<br />
that a population can remain genetically<br />
and demographically healthy<br />
without further importation. For the<br />
time being, the “default” criterion<br />
for genetic self-sustainability of zoo<br />
populations is that the captive population<br />
be able to maintain 90% of the<br />
genetic diversity of the wild population<br />
for 100 years without further<br />
imports. The demographic factor is<br />
equally important and is a precondition<br />
for genetic sustainability. Genetic<br />
diversity comes “wrapped up” in<br />
living individuals. A population that is<br />
losing individuals is therefore always<br />
losing gene diversity – when the animals<br />
are gone, the genes are gone.<br />
Are EAZA bird and mammal populations<br />
demographically self-sustainable?<br />
Demographic self-sustainability<br />
implies that, on average, the number<br />
of births and hatches is as high, or<br />
higher, than the number of deaths<br />
(and, where relevant, exports). If<br />
imports into the EU are becoming<br />
(more) restricted, then we will have<br />
to rely on births and hatches in EAZA<br />
collections or high quality private<br />
and/or non-EAZA collections in the<br />
EU to counteract deaths and removals<br />
of individuals from the population<br />
for other reasons. This is easy to say<br />
but hard to track. Although it is encouraging<br />
that the number of EAZA<br />
institutions joining the International<br />
Species Information System (ISIS)<br />
has rapidly increased over the years,<br />
some zoos are not yet members; not<br />
all zoos have entered all their data;<br />
data are not always up to date; and<br />
the origin of individuals is not always<br />
clear. Analysing the EAZA data in ISIS<br />
will therefore be time-consuming and<br />
not always successful. We therefore<br />
decided to evaluate the EAZA EEP<br />
and ESB bird and mammal populations<br />
by utilising the SPARKS studbook<br />
databases. Furthermore, one<br />
would normally expect that more of<br />
the managed populations are selfsustainable<br />
than are non-managed<br />
populations.<br />
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12<br />
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EAZA Sustainability<br />
Methods<br />
A total of 91 bird and 177 mammal<br />
populations were analysed. The<br />
datasets used for analysis were those<br />
submitted to ISIS that were no more<br />
than two years out of date. The<br />
“EAZA.fed” file in SPARKS was used<br />
as a filter to include only individuals<br />
in EAZA institutions in the analysis.<br />
This approach tells us what can be<br />
achieved with only the individuals in<br />
EAZA member institutions.<br />
Those studbooks/programmes that<br />
manage their species at the subspecies<br />
level were analysed at subspecies<br />
level. Hybrids were eliminated from<br />
the analysis. Species or subspecies<br />
that we knew (e.g. from Regional Collection<br />
Plans [RCPs]) were no longer<br />
recommended to be kept in EAZA<br />
institutions were also omitted.<br />
The degree of self-sustainability of<br />
the populations was assessed based<br />
on five criteria. For each population,<br />
a score card was completed showing<br />
how many of the self-sustainability<br />
criteria it failed (Fig. 1):<br />
• Does the population have less than<br />
50 total individuals? <strong>Population</strong>s<br />
with very low numbers of animals<br />
have a high probability of going<br />
extinct purely due to random demographic<br />
events and catastrophes.<br />
Therefore, even without taking<br />
genetics into account (which would<br />
obviously add to the threat), populations<br />
with less than 50 individuals<br />
have a high probability of extinction.<br />
• Is the proportion of breeding<br />
individuals of the total population<br />
lower than 25%? The ratio of the<br />
effective population size (N e ) to<br />
the true population size (N) is an<br />
important indicator of the genetic<br />
and demographic health of a population.<br />
It indicates how “effective”<br />
the true population size can be in<br />
terms of preserving the population.<br />
For example, you might have 500 individuals<br />
right now, but if for some<br />
reason only five of those can breed,<br />
Fig. 1<br />
The Sumatran orangutan (Pongo abelii) was among the bird and mammal species that<br />
did not score on any of the five criteria, implicating that the population is self-sustainable<br />
according to the parameters set in this study.<br />
© Jolirwan bin Takasi<br />
the effective size of the population<br />
would be much smaller and the<br />
situation would be much less secure<br />
than the total population size would<br />
lead you to believe. Important factors<br />
influencing the effective size<br />
of a population are the number of<br />
breeding animals, sex ratio, family<br />
sizes and fluctuations in population<br />
size. Because reliable calculations of<br />
N e created problems for studbooks<br />
with a high proportion of the pedigree<br />
unknown (which was the case<br />
for a large proportion of pedigrees),<br />
we used the number of breeding<br />
animals in the population as a crude<br />
alternative for N e .<br />
WAZA magazine Vol 12/2011<br />
• Is the PM2000 lambda smaller than<br />
1? In other words, is the growth rate<br />
(i.e. lambda) lower than the replacement<br />
rate, or does the population<br />
have a declining projected growth<br />
rate based on the age-specific birth<br />
and mortality rates?<br />
• Is less than 85% pedigree known? If<br />
less than 85% of the overall population’s<br />
pedigree is known, the genetic<br />
calculations are unreliable and it is<br />
not possible to draw conclusions<br />
about the genetic status of the population.<br />
Even if the studbook keeper<br />
or EEP coordinator is somehow able<br />
to improve knowledge about the
WAZA magazine Vol 12/2011 EAZA Sustainability 13<br />
pedigree, this would not necessarily<br />
result in a higher percentage of<br />
gene diversity retained. If the unknown<br />
portions of the pedigree turn<br />
out to be related to already wellrepresented<br />
founder lines, gene<br />
diversity might even decrease.<br />
• Does the population contain less<br />
than 30 known founders? We stated<br />
above that the current “default”<br />
criterion of genetic self-sustainability<br />
for captive populations is the<br />
ability to maintain 90% of the gene<br />
diversity of the wild population<br />
in the captive population for 100<br />
years without new founder imports.<br />
However, since many pedigrees are<br />
more than 15% unknown, a reliable<br />
number for gene diversity retained<br />
could not be calculated (see criterion<br />
4). For that reason, we decided<br />
to use the number of founders in<br />
the known part of the pedigree as<br />
an alternative criterion for genetic<br />
sustainability.<br />
Sampling and genetic theory indicates<br />
that 20 unrelated wild individuals<br />
are sufficient to capture 97.5% of<br />
the gene diversity of the wild population<br />
within the founder population<br />
(Crow & Kimura 1970; De Boer 1989;<br />
Lacy 1994; Frankham et al. 2002). In<br />
practice, however, contributions of<br />
founders to the living descendant<br />
population are uneven and many<br />
founders may have only marginally<br />
contributed to the genetics of the<br />
living descendant population. For<br />
that reason, quite a few more than<br />
20 founders are often necessary. The<br />
cut-off point was set at 30 founders<br />
because most EEPs and ESBs that<br />
had more than 85% pedigree known<br />
and that could maintain 90% of gene<br />
diversity for 100 years had at least 30<br />
founders (and many had more than<br />
that).<br />
In order to calculate the score card<br />
criteria, an MS Excel spread sheet<br />
was created to hold various parameters<br />
for all the bird and mammal<br />
studbooks.<br />
Table 1.<br />
Sustainability summary score card for EAZA bird<br />
and mammal EEP and ESB populations.<br />
Criterion Birds Mammals<br />
(1) <strong>Population</strong> of less than 50 living individuals 36% 28%<br />
(2) Proportion of individuals breeding lower than 25% 73% 25%<br />
(3) PM2000 growth rate lower than 1 (i.e. decline) 37% 16%<br />
(4) Less than 85% of pedigree known 78% 52%<br />
(5) Less than 30 founders 94% 85%<br />
Results<br />
The average bird studbook has the<br />
following characteristics:<br />
• 90 living individuals at<br />
25 institutions in ten countries;<br />
• 40 living females;<br />
• less than 50% of the pedigree<br />
can be traced;<br />
• 21% 30-day mortality,<br />
32% first-year mortality;<br />
• 20% of the population is breeding.<br />
The average mammal studbook has<br />
the following characteristics:<br />
• 128 living individuals<br />
at 27 institutions;<br />
• 69 living females, 55 living males,<br />
four unknown sex individuals;<br />
• 67% of the pedigree can be traced;<br />
• 28% 30-day mortality,<br />
36% first-year mortality;<br />
• 31% of the population is breeding.<br />
In Table 1, the scores for each of the<br />
five self-sustainability criteria are<br />
presented for the bird and mammal<br />
populations. From the table, it<br />
can, for example, be concluded that<br />
36% of the EAZA bird EEP and ESB<br />
populations have less than 50 living<br />
individuals. Or that 52% of the EAZA<br />
mammal EEP and ESB populations<br />
have less than 85% known pedigrees.<br />
Overall, 75% of bird programmes and<br />
30% of mammal programmes fail on<br />
three or more criteria.<br />
Conclusions<br />
Although the results of the mammal<br />
populations are overall somewhat<br />
better than those of the bird populations,<br />
there is still plenty of room and<br />
serious need for improvement. A high<br />
proportion of populations fail two or<br />
more criteria and many programmes<br />
that fail a certain criterion, fail it by<br />
a relatively large margin. In addition,<br />
we are uncertain of the status of the<br />
non-managed bird and mammal taxa,<br />
but it seems likely that the majority of<br />
these populations are in worse shape<br />
than the EEP and ESB populations.<br />
Such a rapid standardised assessment<br />
of a large number of populations<br />
has of course some limitations. For<br />
example:<br />
• Some species may in reality be<br />
managed at world level, whereby<br />
this larger population has to be selfsustainable,<br />
not the EAZA population<br />
by itself.<br />
• Some species-specific characteristics<br />
cause some of the cut-off<br />
points used to be unsuitable for the<br />
species. For example, species with<br />
longer generation times may be<br />
able to be genetically self-sustainable<br />
with fewer founders, while species<br />
with shorter generation times<br />
might need more.<br />
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EAZA Sustainability<br />
• The standardised time period analysed<br />
may miss important events in<br />
a certain population’s history. For<br />
example, a population analysed<br />
from 1980 until the current date<br />
may show a high growth rate for<br />
most of that period, but then a rapid<br />
decrease. The PM2000 growth rate<br />
obtained from a life table based<br />
on that overall time span may<br />
reflect a positive or stable projected<br />
growth rate, whereas in reality the<br />
population is currently declining and<br />
vice versa.<br />
• As with any kind of cut-off point employed,<br />
some species may just miss<br />
the cut-off, which may in reality not<br />
be significant in terms of sustainability.<br />
• Taxon Advisory Groups (TAGs) may<br />
have decided that some populations<br />
do not need to be self-sustainable<br />
according to the criteria used for<br />
this analysis, for example because<br />
they are willing to accept the<br />
increased risk of extinction (the<br />
populations may in some ways be<br />
less important), because further imports<br />
from the wild are still possible<br />
(logistically, ethically, legally) or because<br />
the population represents the<br />
last individuals in the world and no<br />
additional genetic material exists.<br />
Nevertheless, the scale of the<br />
problem suggests that the overall<br />
conclusions regarding the general<br />
level of self-sustainability of bird and<br />
mammal programmes will be little<br />
influenced by a few programmes<br />
shifting position on a few criteria.<br />
Apart from the realisation that many<br />
of EAZA’s managed programmes for<br />
birds and mammals are by and large<br />
not self-sustainable, this analysis has<br />
led to another important realisation.<br />
To be able to truly decide whether or<br />
not EAZA’s breeding programmes are<br />
successful, we should not be measur-<br />
ing whether each population is selfsustainable,<br />
but whether each population<br />
is achieving its specific goals as<br />
outlined by the TAG in the RCP. Only<br />
when it is clear what role each captive<br />
population should play, and what<br />
targets it needs to achieve to fulfil<br />
that role, can each programme be<br />
measured against those targets and<br />
can the level of management necessary<br />
to reach those targets be defined.<br />
This then leads to the realisation that<br />
we lack a sufficiently sound basis for<br />
setting priorities and determining<br />
roles and targets in the RCPs. It is at<br />
present not clear:<br />
• Which species would benefit from<br />
ex situ populations as part of their<br />
conservation strategy, and how to<br />
decide that in a standardised and<br />
transparent way.<br />
• How this decision-making process<br />
may vary depending on whether or<br />
not the species is threatened (and<br />
to what extent), whether or not the<br />
species is already in captivity, how<br />
feasible success is and what resources<br />
it would take, etc.<br />
• How the priorities for conservation<br />
and for other zoo roles (e.g. education,<br />
entertainment, research)<br />
should be balanced.<br />
In collaboration with other regional<br />
zoo associations, WAZA, the Conservation<br />
Breeding Specialist Group<br />
(CBSG) of the Species Survival Commission<br />
(SSC) of the International<br />
Union for Conservation of Nature<br />
(IUCN), other IUCN/SSC Specialist<br />
Groups, ISIS and other conservation<br />
organisations, EAZA is therefore<br />
playing an active role in the various<br />
initiatives that are currently underway<br />
to create the necessary methods,<br />
tools and paradigm shifts to ensure<br />
that we increase our contribution to<br />
conservation through the intensive<br />
management of populations, and<br />
achieve more secure long-term populations<br />
for our collections.<br />
Acknowledgements<br />
We would like to thank all bird and<br />
mammal EEP coordinators and ESB<br />
keepers for their cooperation and<br />
their hard work in keeping their datasets<br />
accurate and up-to-date.<br />
References<br />
WAZA magazine Vol 12/2011<br />
• Crow, J. F. & Kimura, M. (1970)<br />
An Introduction to <strong>Population</strong><br />
Genetics Theory. New York, NY:<br />
Harper and Row.<br />
• De Boer, L. E. M. (1989) Genetics<br />
and Breeding Programmes –<br />
Genetic Guidelines and their<br />
Background for EEP Coordinators.<br />
Amsterdam: National Foundation<br />
for Research in Zoological<br />
Gardens.<br />
• Frankham, R., Ballou, J. D. &<br />
Briscoe, D. A. (2002) Introduction<br />
to Conservation Genetics. Cambridge:<br />
Cambridge University<br />
Press.<br />
• Lacy, R. C. (1994) Managing genetic<br />
diversity in captive populations<br />
of animals. In: Restoration<br />
of Endangered Species (ed. by<br />
Bowles, M. L. & Whelan, C. J.), pp.<br />
63–89. Cambridge: Cambridge<br />
University Press.
WAZA magazine Vol 12/2011<br />
Sarah Long 1 *, Candice Dorsey 2 & Paul Boyle 2<br />
Status of Association of Zoos<br />
and Aquariums Cooperatively<br />
Managed <strong>Population</strong>s<br />
Introduction<br />
The Association of Zoos and Aquariums<br />
(AZA) is one of the many zoo<br />
associations worldwide that is<br />
undergoing a renewed focus on the<br />
sustainability of its managed populations.<br />
Sustainability is generally<br />
characterised by population biologists<br />
as the ability of a population to<br />
maintain a stable size and healthy<br />
age structure through reproduction<br />
(if self-sustaining) or other means<br />
(importation from private facilities,<br />
other regions or the wild). Genetic<br />
diversity is often measured as a component<br />
of population viability, as<br />
genetically diverse populations are<br />
likely to be more resilient in adapting<br />
to environmental change and avoiding<br />
the negative effects of inbreeding<br />
depression (Frankham et al. 2002).<br />
Maintaining both demographic<br />
stability and gene diversity have long<br />
been part of cooperatively managed<br />
programmes in zoos and aquariums,<br />
including AZA’s Species Survival Plan®<br />
(SSP) and <strong>Population</strong> <strong>Management</strong><br />
Plan (PMP) programmes. Here, we<br />
present an examination of the current<br />
demographic and genetic status of<br />
AZA cooperatively managed Animal<br />
Programmes and an assessment of<br />
key indicators of the viability of these<br />
populations.<br />
1 <strong>Population</strong> <strong>Management</strong> Center,<br />
Lincoln Park Zoo, Chicago, IL, USA<br />
2 Association of Zoos and Aquariums,<br />
Silver Spring, MD, USA<br />
* E-mail for correspondence:<br />
slong@lpzoo.org<br />
As in other regions, population management<br />
in AZA depends upon a network<br />
of volunteer studbook keepers<br />
and species coordinators to collect,<br />
compile and validate pedigrees and<br />
life histories (birth/hatch dates and<br />
locations, transfer events, death<br />
dates and locations) for each individual<br />
of a cooperatively managed population<br />
and to coordinate animal and<br />
institutional needs with population<br />
goals. AZA is unique among regional<br />
zoo associations in having a staff of<br />
full-time professional population<br />
biologists assisting its cooperatively<br />
managed programmes. The AZA <strong>Population</strong><br />
<strong>Management</strong> Center (PMC)<br />
based at Lincoln Park Zoo in Chicago,<br />
IL provides a bridge between studbook<br />
data and the management plan<br />
by helping to improve data quality,<br />
conducting demographic and genetic<br />
analyses and integrating institutional<br />
needs and husbandry information<br />
into breeding and transfer recommendations.<br />
The transformation of<br />
studbook data into management<br />
plans is an essential step in population<br />
management, without which cooperative<br />
efforts towards population<br />
stability and genetic management<br />
are likely to falter. Since its inception<br />
in 2000, the PMC has provided<br />
scientific and logistical support to<br />
approximately 60% of AZA’s Animal<br />
Programmes, producing more than<br />
800 management plans for over 300<br />
populations. Some of the remaining<br />
populations are assisted by a small<br />
number of volunteer advisors, but<br />
over 150 AZA Animal Programmes<br />
have yet to receive any formal population<br />
management advice because<br />
they are newly designated, awaiting<br />
assistance from a population biologist,<br />
or lack a studbook database or<br />
a species coordinator.<br />
Despite all the organisational, institutional<br />
and scientific resources<br />
dedicated to these cooperatively<br />
managed programmes, AZA populations<br />
are facing challenges similar<br />
to zoo populations in other regions –<br />
limited space for expansion, loss of<br />
gene diversity, declining population<br />
sizes, incomplete data with which<br />
to manage the populations – all of<br />
which may threaten the ability of<br />
AZA-accredited zoos to meet their<br />
exhibit, education or conservation<br />
goals with these species. In an attempt<br />
to characterise the viability<br />
of AZA-managed populations, basic<br />
descriptive information was gathered<br />
from studbooks and management<br />
plans for 428 populations and results<br />
of demographic and genetic analyses<br />
conducted by the PMC have been<br />
summarised for 319 populations. Of<br />
particular interest are measures that<br />
provide insight into genetic and demographic<br />
health, such as founding<br />
population size, current population<br />
size, proportion of animals breeding<br />
and recent population growth rates.<br />
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Genetic Status of<br />
AZA <strong>Population</strong>s<br />
Genetic analyses provide estimates<br />
of a population’s gene diversity,<br />
which is an indicator of its adaptive<br />
potential. Estimates of gene diversity<br />
require pedigrees of living animals<br />
tracing back to the wild founders, and<br />
therefore only reasonably complete<br />
pedigrees should be trusted for accurate<br />
genetic calculations. For some<br />
populations with incomplete pedigrees,<br />
the best efforts are made to<br />
develop, in coordination with species<br />
experts, reasonable assumptions<br />
regarding number of founders and<br />
likely relatedness among unknown<br />
pedigreed animals.<br />
Of the populations with reasonably<br />
complete pedigrees for which genetic<br />
calculations could be conducted (264),<br />
the median number of founders is<br />
15, below the minimum 20 founders<br />
generally recommended to provide<br />
a good foundation of gene diversity<br />
(Soulé et al. 1986). Gene diversity<br />
estimates indicate a median of approximately<br />
92% for these populations<br />
as of the most recent analysis<br />
date, and falling to 67% in 100 years.<br />
Approximately 38% of AZA populations<br />
have a current gene diversity<br />
that falls below the 90% benchmark<br />
selected to represent the threshold<br />
between sufficient adaptive potential<br />
and increasing inbreeding risks (Soulé<br />
et al. 1986). While genetic diversity is<br />
often utilised to describe the health<br />
of a population, demographic factors<br />
are more often the cause of immediate<br />
and obvious struggles for population<br />
viability, and act synergistically<br />
to either improve or further decrease<br />
a population’s genetic outlook.<br />
Demographic Status of<br />
AZA <strong>Population</strong>s<br />
The most basic demographic descriptor<br />
is population size. The median<br />
population size of the 428 AZA Animal<br />
Programmes with studbooks or<br />
published breeding and transfer plans<br />
is 66 individuals (Fig. 1). Across species,<br />
approximately 39% of populations<br />
are comprised of 50 or fewer<br />
individuals. <strong>Population</strong>s of this small<br />
size are more vulnerable to variations<br />
in birth/hatch rates, death rates<br />
and birth/hatch sex ratios (Lande<br />
1988), and can more rapidly lose gene<br />
diversity and encounter effects of<br />
inbreeding depression (Frankham et<br />
al. 2002). In addition, non-biological<br />
constraints caused by logistical factors<br />
or lack of cooperation among<br />
participating zoos can easily further<br />
impede the success of populations as<br />
small as these.<br />
The sustainability of closed populations<br />
(i.e. those without access<br />
to additional founders) is heavily<br />
dependent on reproduction. The<br />
proportion of animals breeding in<br />
a population reflects the husbandry<br />
expertise, breeding success and<br />
intensity of management focused<br />
on a species. While these factors are<br />
correlated with the demographic<br />
health of a population, the proportion<br />
of animals breeding is also indicative<br />
of the efficiency at which gene<br />
diversity is retained over time. As<br />
more individuals breed, their cumulative<br />
genetic contributions are passed<br />
on to the next generation, thereby<br />
allowing the population to better<br />
retain gene diversity over time. This<br />
genetic and demographic metric can<br />
be estimated by calculating the ratio<br />
of the number of males and females<br />
with living offspring in the population<br />
(N e , effective population size) to the<br />
total population size (N). Ratios of<br />
N e /N may be constrained by breeding<br />
sex ratios or family sizes (e.g. lower<br />
in populations with polygamous<br />
breeding systems or large groups<br />
with many non-breeding individuals)<br />
Fig. 1<br />
Distribution of population sizes of mammal, bird and reptile/amphibian (“herp”)<br />
programmes cooperatively managed by AZA (N = 428).
WAZA magazine Vol 12/2011<br />
or be temporarily exaggerated in very<br />
small populations with large numbers<br />
of animals breeding. Species with<br />
longer reproductive spans, faster<br />
growth rates, monogamous breeding<br />
systems or fewer limitations on<br />
producing or holding offspring will be<br />
able to achieve higher effective sizes<br />
and therefore achieve better gene<br />
retention.<br />
In 255 AZA populations for which<br />
effective population size ratios (N e /N)<br />
could be calculated, values varied<br />
widely from 0.0 to 0.62 but exhibited<br />
a median of 0.25; in other words, successful<br />
breeders commonly comprise<br />
around 25% of AZA-managed populations.<br />
Trends among taxonomic<br />
groups appear to reflect the previously<br />
mentioned biological and management<br />
differences, with mammal<br />
populations exhibiting slightly higher<br />
effective population sizes (median<br />
N e /N = 0.28, N = 138) and reptiles and<br />
amphibians exhibiting lower effective<br />
population sizes (median N e /N = 0.12,<br />
N = 34); avian populations show intermediate<br />
effective population sizes<br />
(median N e /N = 0.24, N = 93).<br />
The population growth rate, or<br />
change in population size from one<br />
year to the next, is another important<br />
indicator of the demographic<br />
health of a population. Depending<br />
on population goals and available<br />
space, either a stable (approximately<br />
0%) or an increasing growth rate is<br />
desirable for population viability. In<br />
closed populations, the population<br />
size is maintained or increased solely<br />
through reproduction. In open populations,<br />
animals may be brought in<br />
from private facilities, other regions<br />
or the wild to continue to maintain<br />
the population size and offset deaths.<br />
In an examination of recent growth<br />
rates (rates for the five years prior<br />
to the most recent PMC planning<br />
analyses) of 289 AZA cooperatively<br />
managed populations, approximately<br />
40% were decreasing, 15% were stable<br />
and more than 44% were increasing<br />
in population size (Fig. 2). Among<br />
taxonomic groups, birds and reptiles/<br />
amphibians have slightly lower proportions<br />
of decreasing populations<br />
(34% and 35%, respectively) than<br />
mammals (45%).<br />
Fig. 2<br />
Distribution of recent population growth rates (five years prior to analysis date)<br />
for mammal, bird and reptile/amphibian (“herp”) programmes cooperatively<br />
managed by AZA and analysed by the PMC (N = 289).<br />
AZA Sustainability<br />
Improving the Status<br />
of AZA <strong>Population</strong>s<br />
Characterising the current demographic<br />
and genetic health of managed<br />
populations is a transparent<br />
and common way to assess whether<br />
cooperatively managed programmes<br />
are effective. However, there has<br />
been little examination of the process<br />
by which our populations are<br />
managed – through breeding and<br />
transfer recommendations. In the<br />
coming year, AZA will begin to use an<br />
Internet-based system developed at<br />
Lincoln Park Zoo called PMCTrack to<br />
measure the effectiveness of Animal<br />
Programmes by tracking and quantifying<br />
the outcomes of breeding and<br />
transfer recommendations distributed<br />
by SSP programmes. By tracking<br />
outcomes and surveying institutional<br />
representatives to determine the<br />
reasons surrounding why breeding<br />
and transfer recommendations were<br />
not fulfilled, this system may reveal<br />
factors correlated with successfully<br />
managed populations. Eventually,<br />
this information should provide<br />
insight into improving the process of<br />
managing populations and ultimately,<br />
improving the viability of zoo populations<br />
themselves.<br />
While the management and husbandry<br />
issues that foster or hinder population<br />
viability may not be entirely clear,<br />
the basic demographic and genetic<br />
factors that contribute to healthy<br />
populations have been well studied<br />
and are strongly correlated with<br />
space. Assuming that populations<br />
with reasonable founder bases and<br />
effective sizes need to grow to least<br />
150–200 individuals to remain healthy<br />
(Soulé et al. 1986), there is simply not<br />
enough space to keep viable populations<br />
of all species currently managed<br />
in zoos. Exhibits have become larger<br />
and provide space for fewer individuals,<br />
and interest in particular species<br />
varies over time. Multiple species<br />
within a taxonomic group (e.g. old<br />
world monkeys, bears, ungulates)<br />
and across taxonomic groups (e.g.<br />
canids, felids) often compete for the<br />
same space. While managers wait for<br />
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additional facilities and resources, the<br />
age structures of these populations<br />
become destabilised as breeding is<br />
decreased and individuals age and<br />
become reproductively senescent.<br />
Rather than being left to chance<br />
or whim, a prioritisation system is<br />
desperately needed to select the<br />
species that zoos find most important<br />
for achieving their missions (e.g.<br />
conservation efforts, education goals,<br />
exhibit needs) and to phase out the<br />
species that are not serving a role valued<br />
by the majority of zoos. The zoo<br />
community should critically examine<br />
cooperatively managed populations<br />
and other species held in zoos, clarify<br />
the roles of these populations, define<br />
specific goals and outline realistic objectives<br />
required for the populations<br />
to meet those goals. Regional Collection<br />
Plans (RCPs) have been used in<br />
multiple zoo regions to recommend<br />
and prioritise cooperatively managed<br />
species, typically organised at the<br />
level of taxonomic orders. However,<br />
it may be more useful to examine<br />
species outside of taxonomic groupings<br />
and with an eye towards functional<br />
categories (e.g. exhibit needs,<br />
behavioural requirements, education<br />
messaging), as space at modern zoos<br />
is often fluid with the same exhibit<br />
being capable of housing different<br />
species across multiple orders.<br />
Although quantifying the space available<br />
to hold species is notoriously difficult,<br />
space assessments and interest<br />
need to be part of any prioritisation<br />
scheme so that realistic goals can<br />
be set. RCPs and other such species<br />
prioritisation schemes may then<br />
consider many factors including, but<br />
not limited to, the number of holding<br />
institutions, exhibit and education<br />
value, conservation status, husbandry<br />
expertise and success, costs and<br />
a connection to in situ conservation<br />
programmes.<br />
In addition to better management<br />
tools and metrics to assess and prioritise<br />
populations, greater attention to<br />
removing barriers to global cooperation<br />
is needed. In particular, as the<br />
scientific community recognises the<br />
vital role of zoos in protecting biodiversity<br />
(Conde et al. 2011), it is crucial<br />
that governments and regulators<br />
recognise the importance of moving<br />
animals and gametes for building<br />
sustainable zoological populations<br />
and respond with more favourable<br />
permitting processes if our potential<br />
is to be fully realised.<br />
While this summary of the status of<br />
AZA Animal Programmes may highlight<br />
the demographic and genetic<br />
challenges that these populations<br />
face, it may also serve to illustrate the<br />
biases of human perception and the<br />
tendency to nostalgically view the<br />
past in an unrealistic positive light.<br />
For most of the demographic and<br />
genetic indicators discussed, there<br />
are as many populations doing well as<br />
there are doing poorly. It may be that<br />
what is currently being observed is<br />
a natural waxing and waning of species<br />
based on existing conditions (e.g.<br />
space, interest, availability). Species<br />
that were once common and familiar<br />
in zoos of a prior generation may no<br />
longer be suitable or sustainable in<br />
modern zoos that are facing increasing<br />
barriers to importing animals<br />
from other regions and are building<br />
larger, more naturalistic, mixedspecies<br />
exhibits that provide space for<br />
fewer individuals. As exhibits increase<br />
in size to meet animal welfare and<br />
exhibit needs, the number of species<br />
that zoos can maintain at a sustainable<br />
population size decreases. If we<br />
try to come to terms with the realities<br />
of modern zoos and continue to examine<br />
the reasons for both successes<br />
and failures, we will find that many<br />
species thrive in these conditions.<br />
By shifting management priorities<br />
in response to these variables, we<br />
may find that we can tip the balance<br />
towards creating sustainable zoo<br />
populations for generations to come.<br />
References<br />
• Conde, D. A., Flesness, N., Colchero,<br />
F., Jones, O. R. & Scheuerlein,<br />
A. (2011) An emerging role<br />
of zoos to conserve biodiversity.<br />
Science 331: 1390–1391.<br />
• Frankham, R., Ballou, J. D. &<br />
Briscoe, D. A. (2002) Introduction<br />
to Conservation Genetics. Cambridge:<br />
Cambridge University<br />
Press.<br />
• Lacy, R. C. (1997) Importance of<br />
genetic variation to the viability<br />
of mammalian populations. Journal<br />
of Mammalogy 78: 320–335.<br />
• Lande, R. (1988) Genetics and<br />
demography in biological conservation.<br />
Science 241: 1455–1460.<br />
• Soulé, M., Gilpin, M., Conway, W.<br />
& Foose, T. (1986): The millennium<br />
ark: how long a voyage,<br />
how many staterooms, how<br />
many passengers? Zoo Biology 5:<br />
101–113.
WAZA magazine Vol 12/2011<br />
Jonathan D. Ballou 1 * & Kathy Traylor-Holzer 2<br />
Captive <strong>Population</strong>s<br />
and Genetic Sustainability<br />
Introduction<br />
Conservation biologists have long<br />
been interested in the questions of<br />
population viability and sustainability.<br />
The concept of Minimum Viable<br />
<strong>Population</strong> (MVP) size was first developed<br />
to answer the question of how<br />
large a population needs to be to survive.<br />
Quantitatively, MVP is usually<br />
expressed as: “How large does this<br />
population need to be to have 95%<br />
(or some similar percentage) chance<br />
of surviving for 100 years (or some<br />
moderately extended timeframe)?”<br />
Computer modelling (population viability<br />
analysis [PVA]) is typically used<br />
to answer this question, the reliability<br />
of which critically depends on the<br />
amount of detailed data available for<br />
the population. PVA has now become<br />
a standard tool for use in wildlife<br />
conservation.<br />
1 Smithsonian Conservation<br />
Biology Institute,<br />
Washington, DC, USA<br />
2 IUCN/SSC Conservation<br />
Breeding Specialist Group,<br />
Apple Valley, MN, USA<br />
* E-mail for correspondence:<br />
ballouj@si.edu<br />
Soon after the development of<br />
organised captive breeding programmes<br />
in the early 1980s (e.g.<br />
the European Endangered Species<br />
Programme [EEP] of the European<br />
Association of Zoos and Aquaria<br />
[EAZA] and the Species Survival<br />
Plan [SSP] of the Association of<br />
Zoos and Aquariums [AZA] in North<br />
America), zoo biologists also began<br />
wondering about MVPs for captive<br />
populations. How large should our<br />
captive populations be? We asked<br />
a number of prominent conservation,<br />
wildlife and zoo biologists to address<br />
this question at a workshop hosted<br />
by the Smithsonian National Zoo’s<br />
Conservation and Research Center<br />
in 1986. Their recommendation was:<br />
large enough to maintain 90% of the<br />
source population’s genetic diversity<br />
for 200 years (Soulé et al. 1986). The<br />
authors clearly recognised that these<br />
metrics were somewhat arbitrary,<br />
but nevertheless felt that they were<br />
in the right ballpark. Ninety percent<br />
because this represents “the zone<br />
between a potentially damaging and<br />
a tolerable loss of heterozygosity”.<br />
Potentially damaging because a loss<br />
of 10% of the genetic diversity is<br />
roughly equivalent to an increase in<br />
the average inbreeding coefficient in<br />
the population of 10% and approaches<br />
the level at which individuals are as<br />
related as half siblings, and we know<br />
that inbreeding decreases the health<br />
of populations (Frankham et al. 2010).<br />
200 years because it “is a reasonably<br />
conservative temporal horizon…<br />
A longer time ignores the exponential<br />
rate of progress in biological technology”.<br />
The reference to biotechnology<br />
being the benefits of realised<br />
and expected future advances in the<br />
science of storing and regenerating<br />
embryonic cells, and hence a lesser<br />
need for living captive populations to<br />
act as genetic reservoirs for threatened<br />
species. The authors allowed<br />
for disagreement with these metrics<br />
and proposed them as a first step in<br />
the process of determining MVPs<br />
for captive populations. Additionally,<br />
while the metrics are genetic, it was<br />
assumed that genetic criteria for viability<br />
would be stricter than demographic<br />
criteria, and any population<br />
that satisfies the genetic goals would<br />
very likely satisfy any demographic<br />
goals as well (such as those above for<br />
MVPs).<br />
19<br />
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20 Genetics<br />
WAZA magazine Vol 12/2011<br />
»<br />
Size of Captive<br />
<strong>Population</strong>s<br />
So, how large do populations need<br />
to be to meet the “90%/200 Year”<br />
goal? It turns out they need to be<br />
pretty large. The size depends on<br />
the generation length of the species<br />
(the shorter the generation<br />
length, the larger the size required),<br />
number of founders (fewer founders<br />
require a larger population size), how<br />
rapidly the population can grow (slow<br />
growth requires a larger size) and<br />
how well the population has been<br />
and will be managed (the less intensively,<br />
the larger the size required).<br />
For example, to meet this goal the<br />
golden lion tamarin (Leontopithecus<br />
rosalia) population (generation length<br />
of six years, population growth rate<br />
potentially 8% per year, 47 founders –<br />
which is an unusually large number<br />
of founders) would need to grow to<br />
and maintain over 850 individuals.<br />
A species with similar characteristics<br />
except with a generation length of<br />
three years would require over 1,800<br />
individuals (Fig. 1). This is one of the<br />
rare cases in conservation where species<br />
with longer generation lengths<br />
have an advantage; since gene<br />
diversity is potentially lost during<br />
reproduction with each generation,<br />
species with longer generation times<br />
will experience fewer generations<br />
and therefore less genetic loss over<br />
the same time period. These required<br />
population sizes are quite large given<br />
the number of species that rely on<br />
conservation breeding as a core part<br />
of their conservation planning. Given<br />
the limited resources of zoos, managing<br />
larger populations means conserving<br />
fewer species, leading to hard<br />
decisions regarding which species to<br />
conserve and which to abandon.<br />
It was for this reason that in the<br />
mid-1990s, AZA modified their recommended<br />
goals to retain 90% of the<br />
source population’s gene diversity<br />
for only 100 years. There simply was<br />
not enough space for enough species<br />
to meet the 200-year criterion, thus<br />
Fig. 1<br />
<strong>Population</strong> size required to maintain 90% of genetic diversity for 200 years. Species like the<br />
golden lion tamarin (generation length of six years) requires about 850 individuals;<br />
a species with similar characteristics, but a three-year generation length,<br />
would require about 1,800 individuals.<br />
Fig. 2<br />
<strong>Population</strong> size required to maintain 90% of genetic diversity for 100 years for different<br />
species (modified from Frankham et al. 2010). <strong>Population</strong> sizes for species with very<br />
short generation lengths (e.g. amphibians) may require extremely large<br />
population sizes to meet this goal.<br />
sustainability goals were relaxed.<br />
This revision makes a substantial<br />
difference. In the golden lion tamarin<br />
example above, meeting the 100-year<br />
goal “only” requires a population of<br />
about 420 rather than 850 individuals.<br />
Fig. 2 shows the approximate popula-<br />
tion sizes needed for species of different<br />
generation lengths (making some<br />
simplifying assumptions).
WAZA magazine Vol 12/2011<br />
The revised “90%/100 Year” goal is<br />
now used regularly for population<br />
planning in conservation breeding<br />
programmes, although a majority of<br />
the officially recognised programmes<br />
do not have sufficient space to meet<br />
even this objective (Baker 2007; Lees<br />
& Wilcken 2009). Nevertheless, it is<br />
typically accepted as the standard towards<br />
which programmes strive. For<br />
example, AZA has even recently used<br />
it as a primary criterion upon which to<br />
base their new categorisation of their<br />
breeding programmes (e.g. “green”<br />
programmes are those that appear to<br />
be able to reach that goal). Thus, the<br />
goal of “90% for 100 Years” arguably<br />
seems to have become an operational<br />
definition of sustainability for<br />
captive populations.<br />
Genetic Sustainability<br />
of Captive <strong>Population</strong>s<br />
But is “90%/100 Year” really a sustainability<br />
goal? As Robert Lacy<br />
reminded us at a recent workshop<br />
on Intensively Managed <strong>Population</strong>s<br />
for Conservation in San Diego in<br />
December 2010, no, it is not. In fact,<br />
it is the opposite. Accepting a 10%<br />
loss and setting a timeframe of 100<br />
years are both counter to the concept<br />
of sustainability. Depending on the<br />
source, sustainable is defined as being<br />
able to be maintained at a certain<br />
rate or level or by avoiding depletion<br />
of a resource. Tolerating a 10% loss<br />
in the gene pool per century is hardly<br />
sustainable. And what happens in<br />
the year 2111, 100 years from now?<br />
Can we count on the technology to<br />
which Soulé et al. (1986) referred to<br />
be in place? Advances have not been<br />
as rapid as had been predicted. Thus,<br />
the “90%/100 Year” goal is certainly<br />
not a sustainability goal, but rather<br />
a goal that specifically allows for loss,<br />
acknowledging depletion.<br />
If the “90%/100 Year” goal is not a genetically<br />
sustainable goal, then what<br />
is? Conservation geneticists have<br />
debated this extensively (Frankham<br />
et al. 2010). With sustainability being<br />
defined as maintaining a population<br />
large enough so that genetic diversity<br />
is not depleted, then the population<br />
has to be large enough so that the<br />
rate of loss of gene diversity due to<br />
genetic drift (i.e. the random process<br />
of passing genes from parents to<br />
offspring, causing changes in gene<br />
frequencies between generations) is<br />
offset by the rate of increase in genetic<br />
diversity, added via mutations<br />
(the ultimate source of all genetic<br />
variation). Since mutation rates are<br />
very low (e.g. 10 -4 to 10 -5 per locus<br />
per generation for microsatellite<br />
loci; Frankham et al. 2010), the rate<br />
of loss due to genetic drift has to be<br />
correspondingly very low. And since<br />
genetic drift is inversely proportional<br />
to population size, the population<br />
sizes have to be very large.<br />
In genetics, population size is best<br />
expressed as an effective population<br />
size (N e ), defined as the number of<br />
individuals in an ideal population that<br />
loses genetic diversity at the same<br />
rate as the real population. An ideal<br />
population is a theoretical population<br />
that breeds randomly, and all animals<br />
can breed with each other and with<br />
themselves. It is a useful concept because<br />
we can accurately predict, using<br />
population genetics theory, how<br />
the genes in an ideal population will<br />
behave under varying conditions. To<br />
understand the genetics of real populations,<br />
we compare them to ideal<br />
populations. For example, if a population<br />
of 200 wombats loses genetic<br />
diversity at the same rate as an ideal<br />
population of size 52, then we say the<br />
effective size of the wombat population<br />
is 52. The wombat population<br />
is behaving like an ideal population<br />
of 52. So it is a population’s effective<br />
size that determines how it behaves<br />
genetically, not its actual census size.<br />
How N e is calculated is beyond the<br />
scope of this article, but N e can be estimated<br />
for most captive populations.<br />
Of particular interest is the ratio of<br />
a population’s effective size and its<br />
census size (N e /N), which allows one<br />
to calculate a population’s census size<br />
given its effective size, and vice versa.<br />
Genetics<br />
To return to the question of how<br />
large populations need to be to be<br />
genetically sustainable (i.e. suffer no<br />
loss of genetic diversity), the answer<br />
appears to be between N e of 500 and<br />
5,000 (Frankham et al. 2010). This is<br />
regardless of whether the population<br />
is in the wild or captivity. What does<br />
depend on whether the population is<br />
wild or captive is how its effective size<br />
translates into its census size. Wild<br />
populations are typically not managed<br />
genetically, have uneven sex ratios,<br />
fluctuate in size and have some<br />
breeders that produce more offspring<br />
than others, all of which decrease<br />
a population’s effective size. Estimates<br />
of effective sizes in wild populations<br />
are on the order of 10% of<br />
census size (N e /N = 0.11; Frankham et<br />
al. 2010). Thus, genetically sustainable<br />
wild populations need to be about<br />
ten times the effective size, or 5,000<br />
to 50,000 individuals. What about<br />
captive populations? Although no extensive<br />
surveys have been conducted,<br />
population management plans typically<br />
report N e /N as being between<br />
0.25 and 0.30 – much higher than wild<br />
populations, primarily because captive<br />
populations do not fluctuate in<br />
size as much as wild populations and,<br />
presumably, because of population<br />
management. Thus, to be genetically<br />
sustainable, captive populations need<br />
to be on the order of 1,700 to 20,000<br />
animals. Clearly this is not an option<br />
for the vast majority of species under<br />
conservation breeding and may be<br />
only possible for invertebrates and<br />
small vertebrates that can be housed<br />
en masse in breeding centres. Our<br />
captive facilities simply do not have<br />
the capacity to maintain genetically<br />
self-sustaining populations. For that<br />
matter, neither do many if not most<br />
wildlife reserves.<br />
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22 Genetics<br />
WAZA magazine Vol 12/2011<br />
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Possible Ways Forward<br />
How do we deal with this challenge?<br />
We need to recognise that conservation<br />
breeding alone cannot maintain<br />
genetically sustainable populations,<br />
and we should not claim that it can.<br />
This includes recognising that the<br />
goal of “90%/100 Years” is not a goal<br />
for sustainability, but a goal that<br />
explicitly recognises our lack of ability<br />
to maintain genetically sustainable<br />
populations. It means that we will be<br />
challenged with genetic deterioration<br />
in captive populations in the form<br />
of accumulating inbreeding depression<br />
and adaptation to captivity, the<br />
former impacting the health and<br />
welfare of our populations and the<br />
latter impacting the utility of these<br />
populations for future conservation<br />
rescue efforts. These are not new<br />
concerns, but they are concerns that<br />
will not dissipate even if we were to<br />
achieve the goal of “90%/100 Years”.<br />
Although these genetic threats will<br />
not necessarily lead to population<br />
extinction, accumulation of enough<br />
inbreeding significantly increases the<br />
chances of this (Frankham et al. 2010).<br />
Given this, we need to do a better<br />
job at conservation breeding. If zoos,<br />
aquariums and related facilities are<br />
to be seen as legitimate contributors<br />
to species conservation, we need<br />
a more successful conservation<br />
breeding model or paradigm. We<br />
need to expand the size and scope<br />
of our populations by managing<br />
multiple, interacting populations.<br />
Conway (2011) calls for sharper focus<br />
of these efforts, including managing<br />
our captive populations mutually with<br />
wild populations. Captive populations<br />
should be managed globally when<br />
possible, not as isolated regional<br />
populations. Integrated management<br />
of multiple populations will increase<br />
census (and therefore effective)<br />
population size and potentially provide<br />
increased genetic diversity, as<br />
compared to smaller, isolated populations.<br />
We also need to manage our<br />
populations more effectively for conservation<br />
– compliance with population<br />
management recommendations<br />
is not what it should be. The current<br />
paradigm of managing a fragmented<br />
captive population among multiple<br />
facilities, each one holding only<br />
a breeding pair, is not working (Baker<br />
2007; Lees & Wilcken 2009; Conway<br />
2011). We have it backwards. Rather<br />
than designing conservation breeding<br />
programmes to meet our public<br />
exhibit zoo-centric infrastructures, as<br />
we do now, we instead need to design<br />
the facilities to meet the goals of<br />
our conservation programmes. This<br />
was done for the black-footed ferret<br />
(Mustela nigripes) conservation breeding<br />
programme with the dedicated<br />
breeding centre at Sybille, WY, and<br />
there are plans to use similar breeding<br />
centres for cheetahs (Acinonyx<br />
jubatus) by the Conservation Centers<br />
for Species Survival (C2S2), a consortium<br />
of North American zoos with<br />
large land holdings.<br />
Ultimately, we need a shift in thinking<br />
– a refocusing and recommitment<br />
by zoos to serve as effective conservation<br />
centres for the world’s threatened<br />
wildlife species. The past year<br />
has seen a series of workshops that<br />
have begun to raise these issues, and<br />
many are poised to begin tackling<br />
these challenges we face. Let’s hope<br />
the momentum continues.<br />
References<br />
• Baker, A. (2007) Animal ambassadors:<br />
an analysis of the effectiveness<br />
and conservation impact of<br />
ex situ breeding efforts. In: Zoos<br />
in the 21st Century: Catalysts for<br />
Conservation? (ed. by Zimmermann,<br />
A., Hatchwell, M., Dickie,<br />
L. A. & West, C.), pp. 139–154.<br />
Cambridge: Cambridge University<br />
Press.<br />
• Conway, W. G. (2011) Buying<br />
time for wild animals with zoos.<br />
Zoo Biology 30: 1–8.<br />
• Frankham, R., Ballou, J. D. &<br />
Briscoe, D. A. (2010) Introduction<br />
to Conservation Genetics, 2nd ed.<br />
Cambridge: Cambridge University<br />
Press.<br />
• Lees, C. M. & Wilcken, J. (2009)<br />
Sustaining the Ark: the challenges<br />
faced by zoos in maintaining<br />
viable populations. International<br />
Zoo Yearbook 43: 6–18.<br />
• Soulé, M., Gilpin, M., Conway, W.<br />
& Foose, T. (1986): The millennium<br />
ark: how long a voyage,<br />
how many staterooms, how<br />
many passengers? Zoo Biology 5:<br />
101–113.
WAZA magazine Vol 12/2011 23<br />
Cheryl S. Asa 1 *, Kathy Traylor-Holzer 2 & Robert C. Lacy 2,3<br />
Mate Choice as a Potential Tool<br />
to Increase <strong>Population</strong> Sustainability<br />
The Sustainability<br />
Problem<br />
The sustainability of populations has<br />
become an important consideration<br />
for the zoo and aquarium community.<br />
In their analysis of 87 zoo mammal<br />
populations, Lees & Wilcken (2009)<br />
found that 52% were not breeding to<br />
replacement and that 67% fell below<br />
the threshold of 200 animals recommended<br />
by Baker (2007). Conway<br />
(2011) pointed out that new policies<br />
and practices in zoo collection management,<br />
including more specialisation<br />
and focused propagation efforts,<br />
are needed if zoos are to fulfil their<br />
conservation potential. Regional zoo<br />
associations are examining possible<br />
reasons for the unsustainability of<br />
their populations, but one clear factor<br />
is the failure of many assigned<br />
pairs to reproduce, often due to pair<br />
incompatibility. The typical reaction<br />
is to assign another breeding partner,<br />
often requiring the transfer of an<br />
animal to or from another location.<br />
This dating game may finally result in<br />
a successful match, but meanwhile<br />
valuable time and reproductive opportunities<br />
are lost.<br />
1 Saint Louis Zoo,<br />
St. Louis, MO, USA<br />
2 IUCN/SSC Conservation<br />
Breeding Specialist Group,<br />
Apple Valley, MN, USA<br />
3 Chicago Zoological Society,<br />
Brookfield, IL, USA<br />
* E-mail for correspondence:<br />
asa@stlzoo.org<br />
Female Choice and<br />
Reproductive Success<br />
In nature, many animals are able to<br />
choose their mates and the importance<br />
of female choice (females<br />
choosing their mates) has been<br />
documented in many different taxa<br />
(Asa et al. 2011). The factors affecting<br />
mate choice are not always apparent,<br />
but allowing animals to choose<br />
can increase pregnancy rates, litter<br />
sizes and offspring survival. There<br />
are many steps in the reproductive<br />
process, from courtship through<br />
rearing young to independence, and<br />
it appears that mate choice can affect<br />
most if not all of them. Most obviously,<br />
compatible pairs are more likely<br />
to copulate. A female that rejects<br />
mating attempts from a particular<br />
male will not conceive unless forced,<br />
but even when forced, females of at<br />
least some species can impede or<br />
prevent reproduction. Best studied<br />
in birds, females that mate with nonpreferred<br />
males can eject sperm or<br />
even influence the ability of sperm to<br />
fertilise ova. Females of some species<br />
influence embryo survival and litter<br />
size by restricting nutrients or differentially<br />
allocating hormones. Females<br />
can also withhold parental care<br />
and affect survival of offspring that<br />
result from non-preferred matings.<br />
Enhancing animal wellbeing and<br />
promotion of natural behaviours are<br />
goals of modern zoos. Allowing animals<br />
to select partners can contribute<br />
to the wellbeing of those individuals<br />
and better simulates their natural<br />
mating behaviour, contributing to<br />
something we sometimes refer to as<br />
the “happy factor”. Happy females<br />
(i.e. happy with their partners) are<br />
more likely to mate, conceive, incubate<br />
or carry a pregnancy to term and<br />
more likely to be good parents, also<br />
improving offspring wellbeing as well<br />
as survival.<br />
If mate choice is important to the<br />
reproductive success of most species,<br />
then preventing choice could<br />
be counterproductive to reaching<br />
programme objectives. The benefits<br />
from mate choice, for example higher<br />
birth or hatching rates and higher<br />
offspring survival plus enhanced<br />
animal wellbeing, are obvious. Higher<br />
reproductive success means higher<br />
probability of sustainability and faster<br />
growth to the population’s target<br />
size, which helps to slow the loss of<br />
genetic diversity. Allowing animals to<br />
exhibit natural reproductive behaviours<br />
also reduces the unintentional<br />
selection for traits that are adaptive<br />
to certain captive environments, but<br />
not adaptive to more natural environments<br />
for the species.<br />
Mate Choice and<br />
<strong>Population</strong> Genetics<br />
However, allowing mate choice is<br />
not without risk and may undermine<br />
genetic goals if animals choose mates<br />
that are genetically over-represented<br />
in the population (Asa et al. 2011).<br />
Numerous studies have shown that<br />
females make good genetic mate<br />
choices in terms of their own individual<br />
fitness and under the conditions<br />
in which they are living. Such choices,<br />
however, may not result in maximum<br />
retention of genetic diversity in the<br />
population, balance founder representation<br />
or avoid loss of adaptations<br />
to wild environments, which are the<br />
primary goals of captive breeding<br />
programmes (Lacy 1994).<br />
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24<br />
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Mate Choice<br />
As many population mangers have<br />
found, the most genetically valuable<br />
animals in the population (i.e. the top<br />
priority animals for breeding) are not<br />
always the most successful breeders.<br />
Concentrating breeding efforts on<br />
such animals can reduce population<br />
growth and even lead to demographic<br />
instability and population decline.<br />
However, ignoring genetic factors<br />
and concentrating on good breeders<br />
only can reduce genetic variability<br />
and long-term population health and<br />
increase adaptation to captive conditions.<br />
Allowing mate choice by offering<br />
multiple genetically acceptable<br />
mates may be one tool to help balance<br />
demographic and genetic needs of<br />
a population and ultimately maintain<br />
higher levels of genetic diversity by<br />
increasing reproductive success while<br />
relaxing the necessity for imposing<br />
rigid genetic management.<br />
Integrating<br />
Mate Choice and<br />
Genetic <strong>Management</strong><br />
The cues mediating mate preferences<br />
have not been determined for many<br />
species, but this need not prevent<br />
incorporating choice into breeding<br />
programmes. The simplest approach<br />
is to provide a female with access to<br />
several males and observe her reactions.<br />
Generally, females approach<br />
and spend more time with or near the<br />
preferred male; in addition, speciestypical<br />
behaviours, such as sniffing<br />
or performing visual displays, may<br />
be apparent. The female can then<br />
be paired with that male for breeding.<br />
To minimise any negative impact<br />
on population genetics, the several<br />
males presented to the female could<br />
be limited to those considered to<br />
be genetically appropriate potential<br />
mates, with the hope that merely<br />
having a choice will be sufficient to<br />
influence her willingness to mate. It<br />
is important to note that sequential<br />
presentation of potential mates is not<br />
equivalent to allowing choice but is<br />
actually sequential mate rejection/<br />
Fig. 1<br />
Male cheetah scent marking on urine collector.<br />
© Regina Mossotti<br />
Fig. 2<br />
Female cheetah investigating male scent dispenser with male urine sample.<br />
© Regina Mossotti<br />
acceptance. Studies have shown that<br />
females have highest reproductive<br />
success when they can assess their<br />
mate options simultaneously.<br />
Housing and management constraints<br />
may limit the number of<br />
males that can be physically presented<br />
simultaneously; the feasibility and<br />
logistics of providing mate options<br />
also varies greatly among species.<br />
Assessing choice by substituting<br />
appropriate cues (proxies) for the<br />
potential mate himself (e.g. scent) is<br />
a possible alternative that has been<br />
successful in animal models ranging<br />
from mice to humans. For example,<br />
the preference of a female mouse is<br />
consistent whether she is presented<br />
with an assortment of males or their<br />
urine sample. Thus, rather than transfer<br />
a potential mate to a new location,<br />
his urine or other scent sample could<br />
WAZA magazine Vol 12/2011<br />
be sent first to assess the female’s<br />
reaction before investing the resources,<br />
time and risk in transferring the<br />
male. As a first step in assessing the<br />
practicality of using urine as a proxy<br />
for the actual male, one of our graduate<br />
students confirmed that female<br />
cheetahs (Acinonyx jubatus) do investigate<br />
male urine samples and<br />
can use urine to distinguish between<br />
males of different genetic relatedness<br />
(Figs. 1 and 2; Mossotti 2010).<br />
Managers might also be able to influence<br />
female choice by manipulating<br />
cues. Females of some species are<br />
more likely to mate with familiar<br />
males, so the scent of a partner that<br />
would fulfil programme goals could<br />
be presented before presenting<br />
the potential mate himself. In other<br />
species, high rates of scent marking<br />
stimulate a female, presumably by
WAZA magazine Vol 12/2011 Mate Choice 25<br />
representing male vigour and territory<br />
ownership, suggesting another<br />
approach to influencing choice. In<br />
some species, dominant males mark<br />
over scent marks of competitors and<br />
females prefer the male that marks<br />
on top. Managers could use this<br />
strategy to create a “winner” by adding<br />
scent samples sequentially so that<br />
scent from the male best for achieving<br />
population goals is added last.<br />
Females also can be influenced by<br />
the behaviour of other females and<br />
may prefer males that other females<br />
have chosen. Thus, appropriate social<br />
groups may facilitate mate acceptance,<br />
even acceptance of males that<br />
might not have been selected were<br />
the females housed individually.<br />
Given the clear importance of mate<br />
choice in so many species, we believe<br />
the zoo community should consider<br />
incorporating choice in captive<br />
breeding programmes. This should<br />
be approached, however, in a careful<br />
and controlled manner. Not only<br />
is the phenomenon of mate choice<br />
very complex, but allowing mate<br />
choice could be challenging, both<br />
the logistics of offering choice and<br />
implementing choice so that it augments<br />
rather than hinders population<br />
management goals.<br />
Recognising the complexity of this<br />
topic, a Mate Choice Symposium was<br />
held at Saint Louis Zoo in March 2010,<br />
where top scientists who study mate<br />
choice came together with zoo population<br />
managers, including studbook<br />
keepers, species coordinators and<br />
population management advisors.<br />
After a series of research presentations<br />
by the scientists summarising<br />
the mechanisms and consequences of<br />
mate choice across a wide variety of<br />
species, taxon-based working groups<br />
discussed the implications of mate<br />
choice, opportunities for incorporating<br />
mate choice in captive management<br />
and potential research projects<br />
to investigate these issues. Participants<br />
identified possible strategies<br />
for incorporating mate choice into<br />
our current breeding programmes,<br />
including: (1) using information on<br />
mate choice to increase the reproductive<br />
success of genetically valuable<br />
animals; (2) providing multiple<br />
genetically acceptable mates rather<br />
than a single mate; (3) developing<br />
methods for assessing mate acceptability<br />
(via testing of odour or other<br />
cues) before actual animal transfer;<br />
and (4) considering alternate breeding<br />
strategies such as specialised<br />
breeding centres or inter-institutional<br />
management that optimises reproductive<br />
success combined with<br />
periodic exchange of individuals.<br />
The results of this symposium along<br />
with two smaller, related workshops<br />
led to the identification of three<br />
proposed research projects that span<br />
a breadth of taxa, breeding systems<br />
and captive management to address<br />
issues related to incorporating mate<br />
choice into zoo-managed programmes.<br />
These studies are designed<br />
to evaluate the effects of allowing<br />
controlled mate choice within the<br />
following populations: a multi-zoo<br />
breeding programme for a highprofile<br />
species (cheetahs), a single-facility<br />
breeding centre (tanagers) and<br />
a controlled experimental population<br />
(mice). Funding is now being sought<br />
to support these proposed projects.<br />
It is hoped that such studies can serve<br />
as models to help guide the effective<br />
use of mate choice in zoo populations.<br />
Allowing choice may improve reproductive<br />
success and, ultimately,<br />
programme effectiveness. A better<br />
understanding of mate choice can<br />
help population managers reach their<br />
goals for viable, genetically healthy<br />
populations, while potentially helping<br />
minimise selective changes to<br />
captivity and providing insight into<br />
developing a more effective breeding<br />
management strategy for captive<br />
animal populations.<br />
Acknowledgements<br />
We thank Regina Mossotti for use of<br />
the cheetah images.<br />
References<br />
• Asa, C. S., Traylor-Holzer, K. &<br />
Lacy, R. C. (2011) Can conservation-breeding<br />
programmes<br />
be improved by incorporating<br />
mate choice? International Zoo<br />
Yearbook 45: 203–212.<br />
• Baker, A. (2007) Animal ambassadors:<br />
an analysis of the effectiveness<br />
and conservation impact of<br />
ex situ breeding efforts. In: Zoos<br />
in the 21st Century: Catalysts for<br />
Conservation? (ed. by Zimmermann,<br />
A., Hatchwell, M., Dickie,<br />
L. A. & West, C.), pp. 139–154.<br />
Cambridge: Cambridge University<br />
Press.<br />
• Conway, W. G. (2011) Buying<br />
time for wild animals with zoos.<br />
Zoo Biology 30: 1–8.<br />
• Lacy, R. C. (1994) Managing genetic<br />
diversity in captive populations<br />
of animals. In: Restoration<br />
of Endangered Species (ed. by<br />
Bowles, M. L. & Whelan, C. J.), pp.<br />
63–89. Cambridge: Cambridge<br />
University Press.<br />
• Lees, C. M. & Wilcken, J. (2009)<br />
Sustaining the Ark: the challenges<br />
faced by zoos in maintaining<br />
viable populations. International<br />
Zoo Yearbook 43: 6–18.<br />
• Mossotti, R. H. (2010) Female<br />
reaction to male urine scents<br />
as a potential indicator of mate<br />
choice in captive cheetahs<br />
(Acinonyx jubatus). MSc thesis,<br />
Southern Illinois University, Carbondale,<br />
IL.
26 WAZA magazine Vol 12/2011<br />
Dalia A. Conde<br />
Zoos Can Lead the Way<br />
with Ex Situ Conservation<br />
1 *, Nate Flesness2 , Fernando Colchero1 , Owen R. Jones1 & Alexander Scheuerlein1 Summary<br />
Zoos can play a key role in the management<br />
of threatened species that<br />
require the support of captive breeding<br />
for their survival. In this sense, it<br />
is important to have an accounting of<br />
how many at-risk species are already<br />
represented in zoos, which can inform<br />
future prioritisation efforts. We<br />
used data from ISIS and the IUCN Red<br />
List of Threatened Species to assess<br />
the conservation status and population<br />
size of terrestrial vertebrates in<br />
ISIS member institutions. Our results<br />
show that 15% of described species<br />
classified as threatened are represented<br />
in ISIS zoos. Zoos already hold<br />
important populations for certain<br />
threatened species, especially for<br />
mammals. However, the number of<br />
threatened birds and their population<br />
sizes are much lower, which is<br />
even more dramatic for amphibians,<br />
although almost one-quarter of their<br />
populations are above 250 individuals.<br />
The implementation of cooperative<br />
captive breeding programmes across<br />
large numbers of institutions is one of<br />
the more demanding actions where<br />
zoos as a global network could play<br />
a key role to support the conservation<br />
of some of the most threatened<br />
species.<br />
1 Max Planck Institute for Demographic<br />
Research, Rostock, Germany<br />
2 International Species Information<br />
System, Eagan, MN, USA<br />
* E-mail for correspondence:<br />
conde@demogr.mpg.de<br />
Introduction<br />
Zoos and aquariums face a major<br />
task if they are to be effective in<br />
preventing the extinction of some<br />
species. Habitat loss, overhunting<br />
and predation and competition from<br />
invasive species are some of the<br />
pressures that are driving species to<br />
extinction. Moreover, it is expected<br />
that these pressures will be exacerbated<br />
by future climate change. As<br />
a result, although the ultimate goal<br />
must be conservation in the species’<br />
natural habitat, captive breeding<br />
programmes may be the only shortterm<br />
solution to avoid the extinction<br />
of those species whose populations<br />
are highly threatened. In fact, captive<br />
breeding played a major role in the recovery<br />
of 13 of the 68 species that had<br />
improved their conservation status<br />
in the last assessment (Hoffmann et<br />
al. 2010; Conde et al. 2011b). Thus, it<br />
is clear that while captive breeding is<br />
not a conservation goal in itself, it can<br />
be an important conservation tool.<br />
Zoos can potentially lead the way<br />
with ex situ conservation efforts<br />
since they hold a large number of<br />
threatened species and employ staff<br />
with extensive experience of captive<br />
breeding techniques. However,<br />
without knowledge of which species,<br />
and how many individuals per species,<br />
zoos hold, it is difficult for the conservation<br />
community to appreciate<br />
the status of their “insurance populations”.<br />
In this article, we outline the<br />
findings from our recent publication<br />
(Conde et al. 2011a), where we carried<br />
out a detailed accounting of zoo<br />
species using the freely available data<br />
from the International Species Information<br />
System (ISIS) and the Red List<br />
of Threatened Species published by<br />
the International Union for Conservation<br />
of Nature (IUCN).<br />
ISIS is an organisation that holds the<br />
most extensive information on zoo<br />
animals, with more than 2.6 million<br />
individuals across more than 800<br />
member institutions. Although ISIS<br />
does not represent all of the world’s<br />
zoos, it has the best data available to<br />
estimate the representation of the<br />
planet’s biodiversity in captivity. In<br />
Conde et al. (2011a), we matched the<br />
species-level data in ISIS zoos with<br />
the latest IUCN Red List data. The<br />
taxonomic matching was done at the<br />
species level for terrestrial vertebrates<br />
(i.e. mammals, birds, reptiles<br />
and amphibians). Where the ISIS and<br />
IUCN taxonomic names differed, we<br />
used the Catalogue of Life for taxonomic<br />
synonyms. The ISIS data were<br />
then mapped to obtain the distribution<br />
of threatened species across ISIS<br />
zoos.
WAZA magazine Vol 12/2011<br />
Terrestrial Vertebrates<br />
in ISIS Zoos<br />
Conde et al. (2011a) found that<br />
one-quarter of the world’s described<br />
bird species and almost 20% of its<br />
mammal species are represented in<br />
ISIS zoos. In contrast, the representation<br />
of reptiles and amphibians is<br />
considerably lower with just 12% and<br />
4%, respectively (Fig. 1). The picture<br />
is slightly different when we focus<br />
solely on threatened species. Mammals<br />
have the highest representation,<br />
with 24%, 23% and 19% of species<br />
classified as Vulnerable, Endangered<br />
and Critically Endangered, respectively<br />
(Fig. 2). Although the bird collections<br />
account for one-quarter of all<br />
known species, the representation of<br />
threatened species is lower (Vulnerable<br />
= 17%, Endangered = 17%, Critically<br />
Endangered = 9%). However, the<br />
lowest representation of threatened<br />
species is for amphibians, with only<br />
4%, 2% and 3% of species classified as<br />
Vulnerable, Endangered and Critically<br />
Endangered, respectively (41%<br />
of amphibian species are threatened<br />
and ISIS zoos hold only 4% of all<br />
described amphibian species). IUCN<br />
has so far only assessed the conservation<br />
status of 1,672 of the 9,205<br />
described reptile species. From this<br />
incomplete survey, zoos hold 37%,<br />
28% and 51% of species classified as<br />
Vulnerable, Endangered and Critically<br />
Endangered, respectively. As a whole,<br />
roughly one in seven threatened species<br />
of terrestrial vertebrates (15%)<br />
are represented in ISIS zoos.<br />
Although individual zoos usually<br />
do not hold large numbers of individuals<br />
of particular species of conservation<br />
concern, zoos as a global network<br />
hold important populations for<br />
some of the more highly threatened<br />
species. For example, almost onequarter<br />
of the amphibian populations<br />
and 21% of the mammal populations<br />
include more than 250 individuals<br />
worldwide (Fig. 2). The figure is<br />
smaller for bird and reptile populations;<br />
only 8% and 6%, respectively,<br />
exceed 250 individuals.<br />
Fig. 1<br />
The number of terrestrial vertebrates in ISIS zoos compared<br />
to the number of described species.<br />
Threatened Species<br />
The distribution of threatened species<br />
among the world’s ISIS zoos does<br />
not coincide with the distribution of<br />
threatened species in the wild (Fig. 3).<br />
Zoos that hold most threatened species<br />
are concentrated in Europe and<br />
North America, while most of the<br />
wild populations of threatened species<br />
are concentrated in the tropics.<br />
However, it is important to emphasise<br />
that this map only shows species<br />
richness and does not account for the<br />
number of individuals per species.<br />
Consequently, zoos that hold a large<br />
number of species, albeit populations<br />
consisting of few individuals, would<br />
rank higher (brighter on this map)<br />
than zoos having small numbers of<br />
species with large population sizes.<br />
In this sense, Fig. 3 only shows the<br />
distribution of threatened species<br />
across zoos and it should not be seen<br />
as a measure of how zoos contribute<br />
to conservation.<br />
27<br />
»
28 Threatened Species<br />
WAZA magazine Vol 12/2011<br />
»<br />
Fig. 2<br />
Endangered species in zoos. Top: the number of species organised by IUCN Red List status (colour bars) and the number<br />
of those species that are in ISIS zoos (black bars). Bottom: the number of individuals for all species represented in ISIS<br />
zoos. The vertical broken lines show the boundaries by 250, 50 and 10 individuals. The large numbers of species classified<br />
as Vulnerable and Near Threatened are omitted for clarity (modified from Conde et al. 2011a).<br />
Discussion<br />
Zoos already hold important populations<br />
for certain threatened species;<br />
this is especially so for mammals.<br />
However, zoos are rethinking the<br />
way they should manage their collections<br />
if they want to maximise<br />
efforts for ex situ conservation. For<br />
birds, for example, the total number<br />
of threatened species is low and it is<br />
even lower considering the number<br />
of individuals in highly threatened<br />
categories, with only 8% of them<br />
above 250 individuals; the figure is<br />
similar for reptiles. Although zoos<br />
have significantly increased their<br />
collection holdings for amphibians, as<br />
a result of the amphibian crisis, they<br />
can focus on further increasing these<br />
collections. As well it may be advisable<br />
for particular zoos to specialise<br />
their collections on a smaller number<br />
of at-risk taxa rather than aiming to<br />
increase diversity, since it has been<br />
shown that specialisation increases<br />
breeding success (Conway 2011).<br />
Zoos’ contribution to conservation is<br />
not limited to captive breeding, but<br />
as well is growing towards research,<br />
education and the financing of in situ<br />
conservation projects. For example,<br />
members of the WAZA network<br />
collectively are the third largest<br />
contributor to field conservation<br />
projects worldwide after The Nature<br />
Conservancy and the WWF global<br />
network. As a global network, WAZA<br />
zoos and aquariums contribute approximately<br />
US$ 350 million per year<br />
(Gusset & Dick 2011). However, zoos’<br />
contribution towards conservation<br />
could extend further. The accumu-<br />
lated knowledge and data that the<br />
zoo community has collected on the<br />
ISIS network could provide key data<br />
for species for which we lack such<br />
information from the wild, especially<br />
since adequate data from natural<br />
environments are often unavailable<br />
for threatened species. For example,<br />
demographic data such as average<br />
litter size, interval between successive<br />
litters and age at maturity could<br />
be used to fill knowledge gaps for the<br />
development of population viability<br />
analyses. Of course, if these data are<br />
used it should be with caution, since<br />
zoo conditions and the management<br />
of the populations do not mimic the<br />
conditions in the wild. Furthermore,<br />
the data accumulated by the zoo<br />
network in ISIS can be used to assess<br />
selection pressures on the species<br />
in captivity; this could inform which<br />
of these pressures may hamper the
WAZA magazine Vol 12/2011<br />
Fig. 3<br />
Species richness map for threatened mammals, birds and amphibians within ISIS zoos<br />
(top) and in their natural ranges (bottom; modified from Grenyer et al. 2006).<br />
Zoo species richness is represented by points coloured to indicate the number<br />
of species within individual zoos; global species richness corresponds to<br />
the number of species occurring within a 1° latitude by 1° longitude cell.<br />
Reptiles are omitted because the IUCN Red List assessment is still<br />
incomplete (modified from Conde et al. 2011a).<br />
success of their reintroductions into<br />
the wild (Pelletier et al. 2009). In this<br />
sense, studbook keepers have an<br />
important responsibility and a key<br />
role to play since the data they collect<br />
cannot only be helpful for the<br />
management of the species in their<br />
institutions but also for the development<br />
of conservation and management<br />
programmes, such as the<br />
reintroduction of threatened species<br />
into the wild.<br />
The implementation of cooperative<br />
captive breeding programmes across<br />
large numbers of institutions, which<br />
are also referred as Intensively Managed<br />
<strong>Population</strong>s (IMPs), is one of the<br />
more demanding actions where zoos<br />
as a global network could play a key<br />
role. There are many challenges that<br />
must be overcome in order to further<br />
develop these programmes. For<br />
example, one of the first issues will be<br />
to identify which species will need the<br />
assistance of captive breeding before<br />
it is too late to successfully implement<br />
it. The Conservation Breeding<br />
Specialist Group (CBSG) of the IUCN<br />
Species Survival Commission (SSC)<br />
is currently working on guidelines to<br />
identifying those species. Another<br />
challenge is to estimate the capacity<br />
of zoos, both in terms of space and<br />
monetary funds, to manage sustainable<br />
IMPs that could be reintroduced<br />
into the wild over the long term. For<br />
this reason, accurate data on at-risk<br />
species will be essential for the prioritisation<br />
and management of IMPs. In<br />
the future, organisations such as ISIS<br />
will certainly play an active role in<br />
providing critical information support<br />
for IMP programmes among member<br />
zoos across the world; therefore,<br />
there is a need for more institutions<br />
to become part of this global network,<br />
in particular for zoos in countries that<br />
are located in areas with high biodiversity<br />
and high threat, but which are<br />
under-represented in ISIS. Zoos are at<br />
the forefront of global conservation<br />
efforts and, with their combined efforts,<br />
their network has the potential<br />
to make a huge difference.<br />
References<br />
Threatened Species 29<br />
• Conde, D. A., Flesness, N., Colchero,<br />
F., Jones, O. R. & Scheuerlein,<br />
A. (2011a) An emerging role<br />
of zoos to conserve biodiversity.<br />
Science 331: 1390–1391.<br />
• Conde, D. A., Flesness, N., Colchero,<br />
F., Jones, O. R. & Scheuerlein,<br />
A. (2011b) Zoos and Captive<br />
Breeding – Response. Science<br />
332: 1150–1151.<br />
• Conway, W. G. (2011) Buying<br />
time for wild animals with zoos.<br />
Zoo Biology 30: 1–8.<br />
• Grenyer, R., Orme, C. D. L., Jackson,<br />
S. F., Thomas, G. H., Davies,<br />
R. G. et al. (2006) Global distribution<br />
and conservation of rare and<br />
threatened vertebrates. Nature<br />
444: 93–96.<br />
• Gusset, M. & Dick, G. (2011)<br />
The global reach of zoos and<br />
aquariums in visitor numbers and<br />
conservation expenditures. Zoo<br />
Biology 30: in press.<br />
• Hoffmann, M., Hilton-Taylor, C.,<br />
Angulo, A., Böhm, M., Brooks,<br />
T. M. et al. (2010) The impact of<br />
conservation on the status of the<br />
world’s vertebrates. Science 330:<br />
1503–1509.<br />
• Pelletier, F., Réale, D., Watters, J.,<br />
Boakes, E. H. & Garant, D. (2009)<br />
Value of captive populations for<br />
quantitative genetics research.<br />
Trends in Ecology and Evolution<br />
24: 263–270.
30 WAZA magazine Vol 12/2011<br />
Kathy Traylor-Holzer<br />
Identifying Gaps and<br />
Opportunities for Inter-regional<br />
Ex Situ Species <strong>Management</strong><br />
1 *<br />
Summary<br />
A database of 942 studbook and managed<br />
ex situ animal taxa was compiled<br />
and assessed to better understand<br />
the characteristics of managed<br />
species and to be used as a tool for<br />
identifying management opportunities.<br />
Mammals and birds account for<br />
76% of studbook/managed taxa, and<br />
48% of managed taxa are considered<br />
to be threatened by IUCN. Most taxa<br />
are only managed in one region; only<br />
10% of managed taxa are intensively<br />
managed in multiple regions. Regional<br />
differences exist in number of<br />
programmes, taxa and management<br />
intensity. There are 77 threatened<br />
taxa with multiple regional studbooks<br />
that are priority candidates for an<br />
international studbook; similarly, the<br />
database identified 69 threatened<br />
species that are intensively managed<br />
in multiple regions, and should be<br />
further assessed for the potential<br />
benefits and feasibility of interregional<br />
management. Cooperation<br />
and management among regional<br />
programmes may improve the viability<br />
of non-sustainable regional<br />
populations and encourage increased<br />
range country ex situ involvement.<br />
1 IUCN/SSC Conservation<br />
Breeding Specialist Group,<br />
Apple Valley, MN, USA<br />
* E-mail for correspondence:<br />
kathy@cbsg.org<br />
Threatened Species<br />
in Zoos<br />
One-fifth of the 33,468 vertebrate<br />
species assessed in the 2010 Red List<br />
of Threatened Species published by<br />
the International Union for Conservation<br />
of Nature (IUCN) are classified as<br />
threatened (i.e. Critically Endangered,<br />
Endangered or Vulnerable), and the<br />
projected future trend is not optimistic.<br />
The number of threatened vertebrate<br />
species has doubled from 1996<br />
to 2010 – from 3,314 to 6,714 species.<br />
Each year about 52 species of mammals,<br />
birds and amphibians move one<br />
category of threat closer to extinction<br />
(Hoffmann et al. 2010), and 15–37%<br />
of species across sampled regions are<br />
predicted to be “committed to extinction”<br />
due to climate change (Thomas<br />
et al. 2004). Clearly, there is a great<br />
need for increased conservation efforts<br />
to prevent species extinctions,<br />
including the intensive management<br />
of animal populations both in situ<br />
and ex situ.<br />
Intensive management of populations<br />
by zoos and aquariums can play<br />
a myriad of roles that can contribute<br />
to species conservation. Not all threatened<br />
species benefit from ex situ<br />
management, as outlined in the IUCN<br />
Technical Guidelines on the <strong>Management</strong><br />
of Ex Situ <strong>Population</strong>s for Conservation<br />
(IUCN 2002), but for some it<br />
has played a critical conservation role<br />
(Hoffmann et al. 2010). Conde et al.<br />
(2011) estimate that 15% of threatened<br />
terrestrial vertebrate species are<br />
held in zoos (based on the holdings<br />
database of the International Species<br />
Information System [ISIS]), with the<br />
proportion being higher for mammals<br />
and birds. However, over one-half<br />
of these species are held in numbers<br />
totalling fewer than 50 individuals.<br />
These ex situ populations vary greatly<br />
not only in size but in degree of active<br />
monitoring and cooperative management.<br />
<strong>Population</strong>-level management<br />
requires a population database<br />
(studbook), analysis of these data and<br />
application of the results into population<br />
planning to achieve demographic<br />
and genetic goals for the species.<br />
Only 9% of species registered at ISIS<br />
are monitored through an officially<br />
recognised studbook (Oberwemmer<br />
et al., this issue); a smaller portion<br />
of these are managed actively at the<br />
population level. <strong>Population</strong> management<br />
also varies among geographic<br />
regions, as some regional zoo<br />
associations have well-established<br />
administrative and training resources<br />
to promote population management,<br />
while this capacity is still developing<br />
in other regions.<br />
As evidenced by many of the articles<br />
in this issue, much concern has<br />
been expressed regarding the lack<br />
of sustainability of most zoo populations,<br />
including managed populations.<br />
Most management efforts, however,<br />
are conducted at the regional level.<br />
Inter-regional management through<br />
international studbooks and global<br />
management programmes has the<br />
potential to improve viability through<br />
careful metapopulation management<br />
(Leus et al. 2011). Cooperative<br />
programmes among regions also may<br />
help to expand involvement by range<br />
countries or developing zoo associations<br />
in species conservation.
WAZA magazine Vol 12/2011<br />
Zoos hold only a small fraction of the<br />
world’s threatened species, maintain<br />
studbooks for only a portion of these<br />
and actively manage even fewer,<br />
often not effectively as sustainable<br />
populations. A database of species<br />
managed by the regional zoo associations<br />
was compiled to evaluate the<br />
scope of the situation, to assess the<br />
level of management across taxa and<br />
regions and to serve as a potential<br />
tool to identify gaps and opportunities<br />
for inter-regional management in<br />
existing zoo populations.<br />
Managed Species<br />
Database<br />
A database was developed comprised<br />
of 942 taxa monitored (via an active<br />
studbook) and/or actively managed<br />
by regional zoo associations or under<br />
the Amphibian Ark (AArk). Taxa were<br />
listed at the species level except in<br />
a few cases in which multiple regions<br />
manage by subspecies and/or the category<br />
of threat deviated by subspecies.<br />
Partula snails were considered as<br />
one taxon, although approximately<br />
20 species are managed. For each<br />
taxon, the 2010 IUCN Red List status<br />
of threat was recorded along with<br />
the presence of any monitored or<br />
managed population in each of ten<br />
regional zoo associations – AZA<br />
(North America), EAZA (Europe), ZAA<br />
(Australasia), JAZA (Japan), CAZG<br />
(China), SEAZA (South East Asia),<br />
CZA (India), PAAZAB (Africa), ALPZA<br />
(Latin America) and AMACZOOA<br />
(Mesoamerica) – as well as AArk, and<br />
the level of management, using the<br />
following definitions:<br />
• Monitored population: Regional or<br />
international studbook only; this<br />
category also includes ZAA MON1<br />
and MON2 programmes. No population-level<br />
management.<br />
Fig. 1<br />
Percentage of 4,733 IUCN-assessed threatened taxa that are held in ISIS member zoos (14.7%),<br />
have studbooks (8.9%), are managed (7.7%) and are intensively managed (5.4%).<br />
• Managed population: Some<br />
population-level management (e.g.<br />
studbook data analysis, general<br />
recommendations for breeding and/<br />
or transfers); this category includes<br />
AZA <strong>Population</strong> <strong>Management</strong> Plans<br />
(PMPs), EAZA European Studbooks<br />
(ESBs) and low-intensity management<br />
programmes identified by<br />
other regional associations.<br />
• Intensively managed population:<br />
Structured population-level management<br />
(e.g. species management<br />
committee, mandatory breeding<br />
and transfer plan); this category<br />
includes AZA Species Survival Plans<br />
(SSPs), EAZA European Endangered<br />
Species Programmes (EEPs),<br />
ZAA Conservation Programmes<br />
(CPs) and <strong>Population</strong> <strong>Management</strong><br />
Programmes (PMPs), AArk programmes<br />
and other high-intensity<br />
management programmes identified<br />
by other regional associations.<br />
Programme data were obtained either<br />
directly from the zoo associations,<br />
population managers working in the<br />
region and/or association websites,<br />
and are believed to be current as of<br />
early 2011. For analysis purposes, species<br />
listed as Extinct in the Wild were<br />
included among threatened taxa.<br />
Managed Programmes<br />
Managed Species<br />
Characteristics<br />
The majority of the 942 monitored<br />
taxa are mammals (44%) and birds<br />
(31%), with the rest divided among<br />
reptiles (10%), amphibians (7%),<br />
fishes (7%) and invertebrates (< 1%).<br />
Studbooks fall evenly between<br />
threatened (48%) and non-threatened<br />
(45%) taxa, with the remaining<br />
7% of undetermined threat status<br />
(Data Deficient or not assessed by<br />
IUCN). Comparison of this database<br />
with data reported by Conde<br />
et al. (2011) indicate that while 15%<br />
of threatened vertebrate species<br />
(excluding fish) are held in zoos, only<br />
about one-third of these (5.4%) are<br />
intensively managed by zoos (Fig. 1).<br />
31<br />
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32 Managed Programmes<br />
WAZA magazine Vol 12/2011<br />
»<br />
Although species may be held in<br />
multiple regions, most management<br />
takes place within a single region (Table<br />
1). Most (65%) of the 942 monitored<br />
taxa are monitored by a studbook<br />
in only one region, 20% have<br />
multiple regional studbooks and 15%<br />
have international studbooks. For<br />
those taxa that are actively managed,<br />
most are managed in only one region<br />
and only 50 are managed by more<br />
than two regions (mean number of<br />
management programmes = 1.3).<br />
Rates for multiregional management<br />
are higher for threatened (29%) than<br />
for non-threatened (4%) taxa, and<br />
threatened taxa (60%) are managed<br />
more intensively than non-threatened<br />
taxa (27%). About 10% of the<br />
942 monitored taxa are intensively<br />
managed by two or more regions,<br />
most of these being threatened taxa<br />
(N = 79). This means that only 1.6% of<br />
the 4,733 IUCN-assessed threatened<br />
mammal, bird, reptile and amphibian<br />
species are intensively managed by<br />
more than one regional programme.<br />
Regional Differences<br />
Not surprisingly, AZA and EAZA<br />
account for the largest number of actively<br />
managed populations (550 and<br />
358 taxa, respectively) – these are<br />
large regional zoo associations with<br />
long-standing histories of population<br />
management, established population<br />
management advisors and<br />
regular training courses for studbook<br />
keepers and species coordinators.<br />
With smaller capacity, ZAA manages<br />
a smaller number of taxa (N = 83), but<br />
essentially all are managed intensively.<br />
Other regions are quickly<br />
developing studbook and population<br />
management expertise; most notably,<br />
JAZA has made a strong commitment<br />
to population management in recent<br />
years, now maintaining studbooks for<br />
142 species and managing about half<br />
of these on some level. While AZA,<br />
EAZA and ZAA have the longest his-<br />
Table 1.<br />
Number of taxa in the database (N = 942) that have studbooks, management<br />
programmes and intensive management programmes compared to the<br />
number of regional zoo associations coordinating those programmes<br />
(proportion for each column given in parentheses).<br />
Number<br />
Studbook/database <strong>Population</strong>-level<br />
Intensive<br />
of regions<br />
management<br />
management<br />
0 111 (0.12) 549 (0.58)<br />
1 664 (0.70)* 607 (0.64) 296 (0.31)<br />
2 181 (0.19) 174 (0.18) 72 (0.08)<br />
3 58 (0.06) 38 (0.04) 19 (0.02)<br />
4 26 (0.03) 12 (0.01) 6 (0.01)<br />
5 8 (0.01) 0 0<br />
6 5 (0.01) 0 0<br />
*An international studbook is the single database for 49 of these taxa.<br />
torical capacity for population management,<br />
not all taxa are managed<br />
within these three regions. If AArk<br />
programmes are excluded, 110 taxa<br />
are monitored via studbooks outside<br />
of these three regions; of these, 29<br />
taxa are managed and 12 are intensively<br />
managed by the other seven<br />
regional associations (Fig. 2).<br />
Regions differ in other ways in terms<br />
of the taxa they monitor and manage.<br />
All regions hold studbooks or management<br />
programmes unique to their<br />
region – that is, they are the only<br />
region with a studbook or management<br />
programme for that taxon (although<br />
specimens might be present<br />
in other regions). While AZA (N = 309)<br />
and EAZA (N = 144) have the highest<br />
number of unique programmes,<br />
a high percentage of studbook or<br />
programme taxa in ZAA (53%) and<br />
CZA (63%) are exclusively managed<br />
in those regions. CAZG, CZA and<br />
SEAZA have the largest proportion of<br />
their studbook/managed taxa (82%,<br />
67% and 85%, respectively) comprised<br />
of threatened taxa. JAZA (25%)<br />
and PAAZAB (24%) have a larger proportion<br />
of their studbook/managed<br />
taxa represented by reptiles, amphibians<br />
and fishes compared to other<br />
regions. Although AArk programmes<br />
are found worldwide, the majority of<br />
species are being managed in North,<br />
Central and South America. Each<br />
region offers unique contributions to<br />
ex situ population management and<br />
conservation.<br />
Opportunities<br />
for Inter-regional<br />
<strong>Management</strong><br />
This database represents taxa that<br />
are already living in the world’s zoos<br />
and for which some population-level<br />
data exist within one or more studbooks.<br />
Various criteria can be used<br />
to filter these 942 taxa to identify<br />
potential candidates for inter-regional<br />
management in a structured<br />
fashion. For example, among those<br />
801 taxa for which there is currently<br />
no international studbook, there are<br />
77 threatened taxa with two or more<br />
regional studbooks and/or managed<br />
populations, and an additional<br />
11 non-threatened taxa with at least<br />
two intensively managed populations.<br />
These taxa can be easily identified<br />
and are potential priority candidates<br />
for an international studbook. Similarly,<br />
there are 79 threatened taxa<br />
with at least two intensively managed<br />
populations, only ten of which<br />
are currently being managed interregionally<br />
in some coordinated fashion<br />
– the remaining 69 are potential<br />
candidates for global management.
WAZA magazine Vol 12/2011<br />
Fig. 2<br />
Number of taxa for which there are studbooks, low intensity managed populations<br />
or intensively managed populations for each of ten regional zoo associations<br />
as well as the Amphibian Ark.<br />
There are many additional factors<br />
that should be considered, such as<br />
the genetic and demographic status<br />
of the ex situ populations as well as<br />
feasibility issues; however, this tool<br />
can serve to produce a shorter list of<br />
potential candidates that can then<br />
be evaluated more thoroughly with<br />
additional criteria. Currently, this process<br />
is being undertaken by WAZA’s<br />
Committee for <strong>Population</strong> <strong>Management</strong><br />
(CPM). Another potential use of<br />
this database is to quickly identify the<br />
current management level of the ex<br />
situ population within the native geographic<br />
range of each taxon. This in<br />
turn can help to identify gaps where<br />
range country involvement and ex<br />
situ population management can be<br />
encouraged or supported. The expansion<br />
of the database to explicitly<br />
identify range country management<br />
will facilitate this.<br />
Conclusions<br />
Increasingly, intensively managed<br />
populations may be needed to reduce<br />
the risk of extinction for wildlife<br />
species. Only a fraction of currently<br />
threatened species are held by the<br />
world’s zoos, only about half of these<br />
are actively managed and a small<br />
fraction of these are believed to be<br />
sustainable. There are many opportunities<br />
to increase the viability of<br />
regional ex situ populations through<br />
inter-regional databases and interregional<br />
population management.<br />
A database of managed species has<br />
been created as a tool to help identify<br />
opportunities for inter-regional cooperation<br />
and management of existing<br />
studbook species, including increased<br />
involvement of range country ex situ<br />
programmes.<br />
Acknowledgements<br />
I would like to thank the following<br />
individuals for assistance in providing<br />
programme data and assessments:<br />
Kazutoshi Takami, Chris Hibbard,<br />
William van Lint, Christina Henke,<br />
Danny de Man, Xie Zhong, Sally<br />
Walker, Caroline Lees, Roz Wilkins,<br />
Laurie Bingaman Lackey and Virginia<br />
Lindgren. Thanks to Kristin Leus for<br />
providing ideas and comments on<br />
this article.<br />
References<br />
Managed Programmes<br />
• Conde, D. A., Flesness, N., Colchero,<br />
F., Jones, O. R. & Scheuerlein,<br />
A. (2011) An emerging role<br />
of zoos to conserve biodiversity.<br />
Science 331: 1390–1391.<br />
• Hoffmann, M., Hilton-Taylor, C.,<br />
Angulo, A., Böhm, M., Brooks,<br />
T. M. et al. (2010) The impact of<br />
conservation on the status of the<br />
world’s vertebrates. Science 330:<br />
1503–1509.<br />
• IUCN (2002) IUCN Technical<br />
Guidelines on the <strong>Management</strong> of<br />
Ex Situ <strong>Population</strong>s for Conservation.<br />
Gland: IUCN.<br />
• Leus, K., Traylor-Holzer, K. &<br />
Lacy, R. C. (2011) Genetic and<br />
demographic population management<br />
in zoos and aquariums:<br />
recent developments, future<br />
challenges and opportunities for<br />
scientific research. International<br />
Zoo Yearbook 45: 213–225.<br />
• Thomas, C. D., Cameron, A.,<br />
Green, R. E., Bakkenes, M., Beaumont,<br />
L. J. et al. (2004) Extinction<br />
risk from climate change. Nature<br />
427: 145–148.<br />
33
34<br />
Frank Oberwemmer<br />
Which Species Have a Studbook<br />
and How Threatened Are They?<br />
1 *, Laurie Bingaman Lackey2 & Markus Gusset3 Summary<br />
We sought to provide an understanding<br />
of the taxonomic representation<br />
and threat status of species with<br />
a studbook, using data on all studbooks<br />
registered in the ISIS/WAZA<br />
studbook library and data on threat<br />
status from the IUCN Red List of<br />
Threatened Species. Studbooks for<br />
1,027 different species are actively<br />
updated. The majority of species with<br />
an active studbook are vertebrates<br />
(96.3%), mainly comprised of mammals<br />
(48.8%) and birds (31.8%). There<br />
are active studbooks for 1.6% of all<br />
62,574 described vertebrates, including<br />
9.1% of known mammals and<br />
3.3% of known birds. Of those species<br />
with an active studbook, 41.5% are<br />
classified as threatened (i.e. Vulnerable,<br />
Endangered or Critically Endangered)<br />
on the IUCN Red List; 17 out of<br />
34 animal species (50.0%) classified<br />
as Extinct in the Wild have an active<br />
studbook. Of the 989 vertebrates<br />
with an active studbook, 42.6% are<br />
classified as threatened; 8.6% of<br />
25,780 assessed vertebrates classified<br />
as threatened have an active studbook.<br />
Without studbooks, it would be<br />
virtually impossible to scientifically<br />
manage animal populations in human<br />
care.<br />
1 Leipzig Zoo, Leipzig, Germany<br />
2 International Species Information<br />
System, Eagan, MN, USA<br />
3 World Association of Zoos<br />
and Aquariums, Gland, Switzerland<br />
* E-mail for correspondence:<br />
foberwemmer@zoo-leipzig.de<br />
Background<br />
With more than 700 million visitors<br />
worldwide annually and conservation<br />
expenditures in the range of US$ 350<br />
million each year (Gusset & Dick<br />
2011), the world zoo and aquarium<br />
community has the potential to play<br />
an important role in both environmental<br />
education and wildlife<br />
conservation. Indeed, a recent<br />
evaluation of the impact of conservation<br />
on the status of the world’s<br />
vertebrates (Hoffmann et al. 2010)<br />
showed that conservation breeding<br />
in zoos and aquariums has played<br />
a role in the recovery of 28% of the<br />
68 species whose threat status was<br />
reduced according to the Red List of<br />
Threatened Species published by the<br />
International Union for Conservation<br />
of Nature (IUCN). Species previously<br />
classified as Extinct in the Wild that<br />
have improved in status thanks to the<br />
reintroduction of captive-bred animals<br />
include the Przewalski’s horse<br />
(Equus ferus przewalskii), black-footed<br />
ferret (Mustela nigripes) and California<br />
condor (Gymnogyps californianus).<br />
International and regional studbooks<br />
provide the data necessary for coordinating<br />
such conservation breeding<br />
efforts across zoological institutions.<br />
Studbooks are repositories of<br />
pedigree and demographic data on<br />
animals kept in human care internationally<br />
or regionally (Bingaman<br />
Lackey 2010). According to the International<br />
Species Information System<br />
(ISIS), as of July 2010 there were<br />
studbooks for 1,174 different species<br />
included on the international (kept<br />
under the auspices of WAZA) and/or<br />
one of the regional zoo associations’<br />
lists of species to have a studbook<br />
WAZA magazine Vol 12/2011<br />
(a number of species have multiple<br />
regional studbooks assigned). Of the<br />
13,004 species registered at ISIS, 9%<br />
thus have a studbook. Of these, 1,027<br />
are actively updated, while 147 are<br />
no longer being maintained (i.e. they<br />
were “archived”) for various reasons<br />
(e.g. because there is no further need<br />
for the studbook, no captive animals<br />
are left to track or the studbook<br />
keeper could not be replaced).<br />
Zoos and aquariums worldwide keep<br />
at least 15% of threatened terrestrial<br />
vertebrate species (Conde et al. 2011),<br />
but populations of wild animals in<br />
human care are often not viable in<br />
the long term (Lees & Wilcken 2009).<br />
Captive ruminants with an international<br />
studbook have a significantly<br />
higher relative life expectancy than<br />
those without (Müller et al. 2011),<br />
suggesting that the existence of<br />
a studbook may impact conservation<br />
breeding efforts. However, in terms<br />
of their conservation role, we lack<br />
an understanding of the taxonomic<br />
representation and threat status of<br />
species with a studbook. To this end,<br />
we initiated the present study, using<br />
data on all studbooks registered in<br />
the ISIS/WAZA studbook library and<br />
data on threat status from the IUCN<br />
Red List as of July 2010.
WAZA magazine Vol 12/2011 Studbooks 35<br />
Taxonomic<br />
Representation<br />
The majority of species with an active<br />
studbook are vertebrates (96.3%),<br />
mainly comprised of mammals<br />
(48.8%) and birds (31.8%) (Fig. 1).<br />
Vertebrates constitute just over 3%<br />
of the ca. 1.8 million described species<br />
and include 5,498 mammals,<br />
10,027 birds, 9,084 reptiles, 6,638 amphibians<br />
and 31,327 fishes (Hoffmann<br />
et al. 2010). There are thus active<br />
studbooks for 1.6% of all 62,574 described<br />
vertebrates, including 9.1% of<br />
known mammals and 3.3% of known<br />
birds. Studbooks for reptiles were<br />
significantly more often (chi-square<br />
analysis: χ 2 = 8.84, P = 0.003), whereas<br />
studbooks for fishes tended to be less<br />
often (χ 2 = 3.61, P = 0.06), archived<br />
than those for other taxonomic<br />
groups.<br />
Threat Status<br />
Of those species with an active studbook,<br />
41.5% are classified as threatened<br />
(i.e. Vulnerable, Endangered or<br />
Critically Endangered) on the IUCN<br />
Red List (Fig. 2); 17 out of 34 animal<br />
species (50.0%) classified as Extinct<br />
in the Wild have an active studbook.<br />
Of the 989 vertebrates with an active<br />
studbook, 42.6% are classified as<br />
threatened. A recent survey of 25,780<br />
vertebrates represented in the IUCN<br />
Red List (including all mammals, birds,<br />
amphibians, cartilaginous fishes and<br />
statistically representative samples<br />
of reptiles and bony fishes) revealed<br />
that 19% are classified as threatened<br />
(Hoffmann et al. 2010). Thus, 8.6% of<br />
all assessed vertebrates classified as<br />
threatened have an active studbook.<br />
Studbooks for Least Concern and<br />
Near Threatened species tended to<br />
be more often archived than those<br />
for threatened and Extinct in the Wild<br />
species (χ 2 = 3.32, P = 0.07).<br />
Fig. 1<br />
Taxonomic representation of species with a studbook.<br />
Fig. 2<br />
Threat status of species with a studbook (*no entry = species not found on IUCN Red List).<br />
Conservation Role<br />
More than 1,000 different species<br />
have a studbook (cf. Conde et al.<br />
2011). Species with a studbook are<br />
heavily biased towards (charismatic)<br />
vertebrates; around one out of ten<br />
known mammals has a studbook.<br />
While about one-fifth of all assessed<br />
vertebrates are classified as threatened<br />
on the IUCN Red List, about<br />
two-fifths of all studbooks cover<br />
threatened vertebrates; around one<br />
out of ten threatened vertebrates<br />
has a studbook. If species with<br />
a studbook fare better genetically<br />
and demographically (cf. Müller et al.<br />
2011), there is potential for hundreds<br />
of threatened vertebrates to benefit<br />
from the conservation role that<br />
studbooks may play. However, some<br />
taxa, especially amphibians as the<br />
most threatened taxonomic group<br />
of vertebrates (Hoffmann et al. 2010),<br />
are grossly under-represented in<br />
studbooks.<br />
There are reasons other than a species’<br />
threat status that determine<br />
whether a studbook is established<br />
or not, including the following: (1) It<br />
might be considered as important to<br />
keep charismatic vertebrates (e.g. in<br />
order to attract visitors), and thus<br />
to manage these species in the long<br />
term based on a studbook. (2) Even<br />
if a species is common in its native<br />
range, there may be only a small<br />
number of specimens kept in human<br />
care (e.g. for educational or research<br />
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36<br />
»<br />
Studbooks WAZA magazine Vol 12/2011<br />
purposes), which may necessitate<br />
managing this stock collaboratively<br />
for genetic and demographic reasons.<br />
(3) Species not currently threatened<br />
may become so in the future, making<br />
a studbook-based assurance population<br />
potentially valuable. Therefore,<br />
given the limited space in zoos and<br />
aquariums, sound and adaptive collection<br />
planning to prioritise which<br />
species to keep, and for which species<br />
to establish a studbook, is more important<br />
than ever.<br />
There are a number of factors that<br />
may compromise the conservation<br />
role of species with a studbook,<br />
including the following: (1) Not all<br />
of the institutions keeping a given<br />
species provide pedigree and demographic<br />
data for inclusion in the studbook,<br />
reducing the overall number of<br />
animals in a conservation breeding<br />
programme. (2) The system of maintaining<br />
studbooks is based mainly on<br />
voluntary commitment and few institutions<br />
have professional studbook<br />
keepers (or population managers),<br />
thus the value of studbook data is<br />
not fully explored. (3) Recommendations<br />
made by studbook keepers<br />
regarding animal transfers between<br />
institutions are not always followed<br />
or are constrained by legal restrictions,<br />
impairing the effectiveness of<br />
a conservation breeding programme.<br />
All these factors together may diminish<br />
a captive population’s genetic and<br />
demographic viability.<br />
Conclusions<br />
The potential of zoos and aquariums<br />
to assume responsibility for conservation<br />
breeding programmes has been<br />
growing over the years. No other<br />
group of institutions has the scientific<br />
knowledge and practical experience<br />
to keep and breed thousands<br />
of animal species, thereby evidently<br />
contributing to wildlife conservation<br />
(Hoffmann et al. 2010). Nevertheless,<br />
these same institutions have not (yet)<br />
succeeded in managing their populations<br />
sustainably (Lees & Wilcken<br />
2009). This is despite frequent calls to<br />
action over the past 30 years, significant<br />
scientific input and much organisational<br />
effort. Although WAZA has<br />
mandated ISIS with the management<br />
of studbook data, not all institutions<br />
are required by their regional zoo associations<br />
to submit data for inclusion<br />
in the ISIS/WAZA studbook library.<br />
Lees & Wilcken (2009) calculated<br />
that the average population size for<br />
captive vertebrates would increase by<br />
42% if regionally managed populations<br />
were linked up.<br />
To fulfil the full suite of conservation<br />
roles required of animal populations<br />
in human care (Conde et al.<br />
2011), they must be demographically<br />
robust, genetically representative<br />
of wild counterparts and able to<br />
sustain these characteristics for the<br />
foreseeable future. International<br />
and regional studbooks form the<br />
basis of such conservation breeding<br />
efforts. Studbook keepers thus<br />
provide an invaluable service to the<br />
world zoo and aquarium community;<br />
the single most important determinant<br />
of a sound studbook probably is<br />
having a dedicated keeper. However,<br />
it seems that studbook data are not<br />
being adequately translated into<br />
management recommendations and/<br />
or those recommendations are not<br />
being implemented within institutions.<br />
This implies that the system<br />
of maintaining studbooks needs<br />
to move from mere bookkeeping<br />
to proactive population management.<br />
Based on the above, for zoos<br />
and aquariums to be a recognised<br />
conservation force, more professionalism,<br />
compliance and inter-regional<br />
cooperation appear to be advisable.<br />
Acknowledgements<br />
We are grateful to Gerald Dick, Jörg<br />
Junhold and Laura Penn for helpful<br />
comments on this article.<br />
References<br />
• Bingaman Lackey, L. (2010)<br />
Records, studbooks, regional zoo<br />
associations, and ISIS. In: Wild<br />
Mammals in Captivity: Principles<br />
and Techniques for Zoo <strong>Management</strong>,<br />
2nd ed. (ed. by Kleiman, D.<br />
G., Thompson, K. V. & Kirk Baer,<br />
C.), pp. 504–510. Chicago, IL:<br />
University of Chicago Press.<br />
• Conde, D. A., Flesness, N., Colchero,<br />
F., Jones, O. R. & Scheuerlein,<br />
A. (2011) An emerging role<br />
of zoos to conserve biodiversity.<br />
Science 331: 1390–1391.<br />
• Gusset, M. & Dick, G. (2011)<br />
The global reach of zoos and<br />
aquariums in visitor numbers and<br />
conservation expenditures. Zoo<br />
Biology 30: in press.<br />
• Hoffmann, M., Hilton-Taylor, C.,<br />
Angulo, A., Böhm, M., Brooks,<br />
T. M. et al. (2010) The impact of<br />
conservation on the status of the<br />
world’s vertebrates. Science 330:<br />
1503–1509.<br />
• Lees, C. M. & Wilcken, J. (2009)<br />
Sustaining the Ark: the challenges<br />
faced by zoos in maintaining<br />
viable populations. International<br />
Zoo Yearbook 43: 6–18.<br />
• Müller, D. W. H., Bingaman<br />
Lackey, L., Streich, W. J., Fickel,<br />
J., Hatt, J.-M. & Clauss, M. (2011)<br />
Mating system, feeding type and<br />
ex situ conservation effort determine<br />
life expectancy in captive<br />
ruminants. Proceedings of the<br />
Royal Society B 278: 2076–2080.
WAZA magazine Vol 12/2011<br />
Dennis W. H. Müller 1 *, Laurie Bingaman Lackey 2 ,<br />
W. Jürgen Streich 3 , Jörns Fickel 3 , Jean-Michel Hatt 1 & Marcus Clauss 1<br />
How to Measure Husbandry<br />
Success? The Life Expectancy<br />
of Zoo Ruminants<br />
Summary<br />
Relative life expectancy (i.e. the<br />
average life expectancy of a species<br />
expressed as a percentage of the<br />
maximum longevity ever reported for<br />
this species) may describe husbandry<br />
success in captive populations. By<br />
correlating the relative life expectancy<br />
with biological characteristics and<br />
husbandry factors for different species,<br />
reasons for variations in relative<br />
life expectancy can be detected. We<br />
analysed data for 166,901 ruminants<br />
of 78 species and demonstrated<br />
the presence of such a correlation<br />
between relative life expectancy and<br />
percentage grass in the species’ natural<br />
diet (not necessarily the diet fed<br />
in zoos). This suggests that species<br />
adapted to grass (so-called grazers,<br />
such as bison and wildebeest) can be<br />
managed more easily when compared<br />
to species that feed on leaves<br />
and twigs (so-called browsers, such<br />
as giraffe and moose). Another finding<br />
of our analysis is a true success<br />
story of zoo animal management: the<br />
1 Clinic for Zoo Animals, Exotic Pets<br />
and Wildlife, Vetsuisse Faculty,<br />
University of Zurich, Zurich,<br />
Switzerland<br />
2 International Species Information<br />
System, Eagan, MN, USA<br />
3 Leibniz Institute for Zoo and Wildlife<br />
Research, Berlin, Germany<br />
* E-mail for correspondence:<br />
dmueller@vetclinics.uzh.ch<br />
relative life expectancy was higher in<br />
species that were managed by an international<br />
studbook than in species<br />
not managed this way. This highlights<br />
the positive effect of intensive<br />
studbook management on the overall<br />
husbandry success of the respective<br />
species. Translating these results into<br />
husbandry recommendations, our<br />
approach can help to improve zoo<br />
animal husbandry.<br />
Background<br />
Zoo animal husbandry is aimed at<br />
constantly improving husbandry conditions,<br />
provision of veterinary care,<br />
reproductive success and thus ultimately<br />
husbandry success. Important<br />
questions arise from these aims: how<br />
can husbandry success be measured<br />
objectively, and how can we improve<br />
it on the basis of scientific results?<br />
Although some zoological institutions<br />
make a great effort to study various<br />
aspects of wellbeing for certain species,<br />
comparative analyses needed<br />
to determine factors influencing the<br />
husbandry success of different species<br />
in captivity are rare (Mason 2010).<br />
In 2003, WAZA proclaimed the goal<br />
“to exercise the highest standards of<br />
animal welfare”, leading to the question<br />
of how husbandry success and<br />
animal welfare can be measured objectively.<br />
A comparison of life history<br />
parameters such as breeding success<br />
per year or life expectancy between<br />
a zoo population and a wild population<br />
is an option to find out whether<br />
a species fares better in captivity<br />
than in the wild. In comparing three<br />
populations of wild but unhunted<br />
deer species with their respective zoo<br />
populations, we demonstrated that<br />
life expectancies of red deer (Cervus<br />
elaphus) and reindeer (Rangifer<br />
tarandus) were within the same range<br />
or even markedly higher in zoos,<br />
whereas captive roe deer (Capreolus<br />
capreolus) had a shorter life expectancy<br />
than their free-ranging conspecifics<br />
(Müller et al. 2010a).<br />
We believe that the problems in<br />
providing adequate browse to captive<br />
roe deer (a typical browser that feeds<br />
on leaves and twigs) and problems<br />
associated with more crowded<br />
conditions in zoos (as roe deer live<br />
predominantly solitarily in the wild)<br />
may have led to nutritional deficiencies<br />
and increased stress, leading to<br />
shorter life expectancy in captivity.<br />
On the other hand, reindeer and red<br />
deer are naturally socially living and<br />
are both so-called mixed feeders,<br />
adapted to feed moderate amounts<br />
of grass. Thus, they cope well in zoos<br />
and achieve comparatively high life<br />
expectancies. Unfortunately, such<br />
analyses will be restricted to a few<br />
exemplary comparisons, as reliable<br />
data for free-ranging populations are<br />
missing for most species. To test our<br />
hypotheses that the social system<br />
and feeding behaviour of a species<br />
in the wild have an influence on<br />
husbandry success, we conducted an<br />
analysis of the life expectancy of ruminant<br />
species (deer, giraffes, cattle,<br />
antelopes, gazelles, etc.) in zoos.<br />
37<br />
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38 Life Expectancy<br />
WAZA magazine Vol 12/2011<br />
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Comparison of<br />
Life Expectancy<br />
among Ruminants<br />
A comparative analysis of different<br />
species’ life expectancies in captivity<br />
can be used to detect factors that<br />
influence life expectancy in captivity.<br />
Such factors would consequently<br />
have an important impact on husbandry<br />
success and also on animal<br />
welfare. We used data from approximately<br />
167,000 animals representing<br />
78 ruminant species kept in about<br />
850 zoos around the world (data from<br />
the International Species Information<br />
System [ISIS]) to calculate the<br />
life expectancy of a species’ overall<br />
zoo population. Life expectancy of<br />
different species depends on the<br />
body mass of a species – species with<br />
a higher body mass such as bison<br />
(Bison bison) and giraffe (Giraffa<br />
camelopardalis) achieve higher life<br />
expectancies than do smaller species<br />
such as roe deer or gazelles (Gazella<br />
spp.). Comparative analyses of different<br />
species’ life expectancies require<br />
a correction for this effect. This was<br />
done by calculating the relative life<br />
expectancy of a species in captivity.<br />
The average life expectancy of<br />
a species was hereby expressed as<br />
a percentage of the maximum longevity<br />
ever reported for this species.<br />
Ranging from 0–100%, a relative<br />
life expectancy of 0% would denote<br />
the death of all individuals at birth,<br />
whereas a relative life expectancy of<br />
100% would imply that all individuals<br />
reach the maximum longevity for<br />
that species. For example, assuming<br />
an average life expectancy of<br />
80 years and a maximum longevity<br />
of 122 years for women in western<br />
Europe, women nowadays have<br />
a relative life expectancy of 66%. In<br />
zoo ruminants, the relative life expectancy<br />
ranged from 27% for moose<br />
Fig. 1<br />
A boxplot of the relative life expectancy of ruminant species with low amounts of dietary<br />
grass in the wild (browsers) in comparison with species that feed moderate proportions of grass<br />
in the wild (mixed feeders) and species that ingest high proportions of grass in the wild (grazers).<br />
Included are 20 browsers (e.g. moose), 32 mixed feeders (e.g. Alpine ibex [Capra ibex]) and<br />
26 grazers (e.g. bison). From top to bottom, boxplots show the highest value, the value<br />
achieved by 75% of species, the value achieved by 50% of species, the value achieved<br />
by 25% of species and the lowest value of the relative life expectancy.<br />
Note that the relative life expectancy was lowest<br />
in browsing species and highest in grazers.<br />
(Alces alces) to 59% for Arabian oryx<br />
(Oryx leucoryx), with a mean relative<br />
life expectancy of 43% (Müller et al.<br />
2011). We then tested the influence<br />
of several biological parameters (e.g.<br />
feeding behaviour, social system) and<br />
husbandry measures (e.g. keeping of<br />
an international studbook for a species)<br />
on the relative life expectancy.<br />
The relative life expectancy correlates<br />
positively with the percentage<br />
of grass in a species’ natural diet<br />
(not necessarily the diet fed in zoos)<br />
(Müller et al. 2010b, 2011). Browsing<br />
species with a lower percentage of<br />
grass in their natural diet (e.g. giraffe,<br />
moose) had, on average, a lower<br />
relative life expectancy compared<br />
with grazing species (e.g. bison,<br />
wildebeest [Connochaetes taurinus])<br />
that have a high percentage of grass<br />
in their natural diet (Fig. 1). Thus, our<br />
results confirm the general experience<br />
of zoos where browsing species,<br />
evolutionarily adapted to eat leaves<br />
and twigs, have more nutritionrelated<br />
problems than mixed feeders<br />
(with a moderate proportion of grass<br />
in their diet) and grazers. Obviously,<br />
these nutrition-related health problems<br />
have a significant influence on<br />
life expectancy in captivity.<br />
One of the major achievements of<br />
zoos in the last century was the conservation<br />
of species that had become<br />
extinct in the wild, including European<br />
bison (Bison bonasus), Przewalski’s<br />
horse (Equus ferus przewalskii) and<br />
Père David’s deer (Elaphurus davidianus).<br />
A major key to this success was<br />
the cooperation and breeding coordination<br />
of many zoos with international<br />
studbooks. Nowadays, conservation<br />
of endangered species by ex<br />
situ breeding programmes is one of<br />
the most important aims of zoological<br />
institutions (WAZA 2005), and international<br />
studbooks for more than<br />
150 species have been established.<br />
Detailed husbandry recommenda-
WAZA magazine Vol 12/2011<br />
Fig. 2<br />
A boxplot of the relative life expectancy of species that were not managed (N = 64)<br />
and of species that were managed (N = 14) with the help of an international studbook.<br />
In descending order, the boxplots show the highest value, the value achieved by 75%<br />
of species, the value achieved by 50% of species, the value achieved by 25% of species<br />
and the lowest value of the relative life expectancy. Note that species that were<br />
managed with an international studbook had a higher relative life expectancy<br />
compared with species without such management.<br />
tions including spatial requirements,<br />
housing facilities, group size and<br />
composition and feeding regimes are<br />
often an integral part of these studbooks.<br />
The relative life expectancy<br />
was higher in species managed with<br />
the help of an international studbook<br />
kept under the auspices of WAZA (Fig.<br />
2; Müller et al. 2010b, 2011). Consequently,<br />
the success of such intensive<br />
population management seems to be<br />
reflected in the higher life expectancy<br />
of studbook-managed species.<br />
Although it is unknown whether<br />
efforts to reduce inbreeding in<br />
studbook-managed populations<br />
as compared to species without an<br />
international studbook, or the implementation<br />
of detailed husbandry<br />
guidelines, have also contributed to<br />
the higher relative life expectancies<br />
of the relevant species, this finding<br />
should encourage more intensive use<br />
of studbook coordination in additional<br />
species.<br />
Conclusions<br />
Our results identified species that live<br />
under suboptimal husbandry conditions<br />
(e.g. moose); additional efforts<br />
should be undertaken to improve<br />
these. Furthermore, we identified<br />
biological characteristics of species<br />
relevant to their life expectancy in<br />
captivity, such as natural diet, which<br />
should be considered in further<br />
improving husbandry success in zoos.<br />
Finally, we demonstrated that intensively<br />
managing a population with<br />
the help of an international studbook<br />
has a positive effect on the husbandry<br />
success of the respective species.<br />
Acknowledgements<br />
We thank the Georg and Bertha<br />
Schwyzer-Winiker-Stiftung and the<br />
Vontobel-Stiftung for financial support,<br />
WAZA for enabling the data<br />
transfer from ISIS and all participating<br />
zoos for their consistent data<br />
collection.<br />
References<br />
Life Expectancy<br />
• Mason, G. J. (2010) Species differences<br />
in responses to captivity:<br />
stress, welfare and the comparative<br />
method. Trends in Ecology<br />
and Evolution 25: 713–721.<br />
• Müller, D. W. H., Gaillard, J.-M.,<br />
Bingaman Lackey, L., Hatt, J.-M.<br />
& Clauss, M. (2010a) Comparing<br />
life expectancy of three deer<br />
species between captive and wild<br />
populations. European Journal of<br />
Wildlife Research 56: 205–208.<br />
• Müller, D. W. H., Bingaman<br />
Lackey, L., Streich, J., Hatt, J.-M.<br />
& Clauss, M. (2010b) Relevance<br />
of management and feeding<br />
regimens on life expectancy in<br />
captive deer. American Journal of<br />
Veterinary Research 71: 275−280.<br />
• Müller, D. W. H., Bingaman<br />
Lackey, L., Streich, W. J., Fickel,<br />
J., Hatt, J.-M. & Clauss, M. (2011)<br />
Mating system, feeding type and<br />
ex situ conservation effort determine<br />
life expectancy in captive<br />
ruminants. Proceedings of the<br />
Royal Society B 278: 2076–2080.<br />
• WAZA (2005) Building a Future<br />
for Wildlife: The World Zoo and<br />
Aquarium Conservation Strategy.<br />
Berne: WAZA.<br />
39
40 WAZA magazine Vol 12/2011<br />
Anne M. Baker<br />
Intensive <strong>Management</strong><br />
of <strong>Population</strong>s for Conservation<br />
1 , Robert C. Lacy2,3 *, Kristin Leus4,5 & Kathy Traylor-Holzer3 What is an “Intensively<br />
Managed <strong>Population</strong>”?<br />
As habitats are increasingly altered<br />
and wildlife populations impacted by<br />
human activities, more species are<br />
being actively managed to assure<br />
their persistence. This has led to<br />
a new term among conservationists<br />
– Intensively Managed <strong>Population</strong>s<br />
(IMPs). An IMP is one that is<br />
dependent on human care at the<br />
individual and population level for its<br />
persistence (Fig. 1). Ex situ populations<br />
that depend on managers for<br />
food, medical treatment, living space,<br />
protection from predation and access<br />
to mates are clearly intensively<br />
managed. Some wild populations are<br />
reliant on at least some of these kinds<br />
of individual care and would also fall<br />
within the scope of IMPs. <strong>Population</strong>s<br />
living without regular intervention<br />
for individuals but requiring management<br />
at the population level (e.g.<br />
protection from poaching) or habitats<br />
will often be “light managed” or “conservation<br />
dependent” (Cook 2010).<br />
1 Toledo Zoo, Toledo, OH, USA<br />
2 Chicago Zoological Society,<br />
Brookfield, IL, USA<br />
3 IUCN/SSC Conservation<br />
Breeding Specialist Group,<br />
Apple Valley, MN, USA<br />
4 IUCN/SSC Conservation<br />
Breeding Specialist Group Europe,<br />
c/o Copenhagen Zoo, p/a Merksem,<br />
Belgium<br />
5 European Association of Zoos and<br />
Aquaria, Amsterdam, The Netherlands<br />
* E-mail for correspondence:<br />
rlacy@ix.netcom.com<br />
The Opportunity<br />
for Zoos<br />
The opportunity for zoological<br />
institutions to contribute to species<br />
conservation through the long-term<br />
maintenance of populations is very<br />
large. The more than 800 zoos and<br />
aquariums that are members of the<br />
International Species Information<br />
System (ISIS) currently hold more<br />
than 600,000 living specimens of<br />
about 4,000 species of tetrapod vertebrates.<br />
Of these populations, 18%<br />
are currently for those species identified<br />
at some level of conservation risk<br />
in the wild. For mammals and birds,<br />
zoos hold about one-fifth to onequarter<br />
of the species identified by<br />
the International Union for Conservation<br />
of Nature (IUCN) as threatened,<br />
while the numbers are much lower<br />
for reptiles and amphibians (Conde<br />
et al. 2011). However, for about half<br />
of these threatened species, the<br />
total number of individuals held in all<br />
ISIS zoos is fewer than 50 specimens,<br />
a size below which conservationists<br />
do not consider a population to be<br />
viable for even the short term.<br />
Concerns regarding the sustainability<br />
and not fully realised conservation<br />
potential of these zoo populations<br />
led to a workshop on the use of<br />
intensively managed populations for<br />
species conservation held in December<br />
2010 and hosted by San Diego<br />
Zoo. Facilitated by the Conservation<br />
Breeding Specialist Group (CBSG)<br />
of the IUCN Species Survival Commission<br />
(SSC), the workshop was<br />
attended by 45 zoo professionals<br />
from around the world. The purpose<br />
of the workshop was to address the<br />
challenge of insuring that intensive<br />
population management contributes<br />
to species living within healthy ecosystems<br />
in evolving communities.<br />
This workshop involved focused<br />
discussions on those populations that<br />
are being intensively managed for the<br />
conservation of those species. Zoo<br />
populations serve also important educational,<br />
aesthetic and cultural values,<br />
but these roles do not necessarily involve<br />
the maintenance of threatened<br />
taxa. Efficient use of resources might<br />
require that zoo populations that<br />
are used for educational and display<br />
purposes also be breeding populations<br />
of species needing protection<br />
(Conway 2011), and in those cases<br />
the management of the populations<br />
must be adequate for achieving the<br />
species conservation goals as well as<br />
the exhibit goals.
WAZA magazine Vol 12/2011<br />
Fig. 1<br />
Intersections of biodiversity conservation, ex situ zoological and botanical institutions and<br />
intensive management of populations, with examples of the activities that fall within each region.<br />
The centre of overlap between all three circles are those ex situ populations that are being<br />
managed intensively to help achieve their conservation. That region plus the intensively<br />
managed wild populations constitutes the focus of the discussions<br />
on the use of IMPs for conservation.<br />
Working groups tackled aspects of<br />
intensive population management for<br />
species conservation, from identifying<br />
priority species for management<br />
to improving management effectiveness<br />
and increasing collaboration.<br />
The following goal encapsulates<br />
much of what participants believe<br />
zoos need to achieve: The world<br />
zoo and aquarium communities are,<br />
and are acknowledged as, effective<br />
conservation partners in the context of<br />
integrated conservation strategies that<br />
include intensive population management.<br />
To work towards this goal, we must:<br />
• Change the current paradigm of<br />
the ways zoos contribute to species<br />
conservation by committing to<br />
conservation missions and adopting<br />
appropriate business models to<br />
achieve this.<br />
• Incorporate IMPs as potential<br />
effective conservation tools into<br />
holistic species conservation strategies,<br />
increase collaboration with<br />
conservation partners and improve<br />
understanding of the role of IMPs in<br />
conservation.<br />
• Improve the viability and success of<br />
long-term IMP programmes, ensuring<br />
that each species has a precise<br />
and appropriate management plan<br />
and adequate resources to achieve<br />
its roles.<br />
• Improve the success of species conservation<br />
programmes by optimally<br />
utilising populations along a management<br />
continuum, including exploration<br />
of alternative approaches<br />
to population management and<br />
expanding metapopulation strategies<br />
for managing multiple populations<br />
effectively.<br />
Intensively Managed <strong>Population</strong>s<br />
The Challenges<br />
Regional zoo associations coordinate<br />
the collaborative management of<br />
about 800 species, in programmes<br />
such as the Species Survival Plan<br />
(SSP) of the Association of Zoos and<br />
Aquariums (AZA) in North America,<br />
the European Endangered Species<br />
Programme (EEP) of the European<br />
Association of Zoos and Aquaria<br />
(EAZA), the Australasian Species<br />
<strong>Management</strong> Program (ASMP) of the<br />
Zoo and Aquarium Association (ZAA)<br />
Australasia, and others. Often, however,<br />
these populations are managed<br />
in isolation and ex situ efforts often<br />
are not integrated with in situ conservation<br />
needs or activities, even for<br />
endangered species. Although we in<br />
the zoo community have convinced<br />
ourselves, our staff and our public<br />
that our managed programmes<br />
serve important conservation roles<br />
for those species, rarely can this be<br />
documented to be the case.<br />
<strong>Population</strong> goals for managed<br />
taxa are usually defined in terms of<br />
genetics and demographics, rather<br />
than in terms of supporting species<br />
conservation. Even given these<br />
limited goals, most managed zoo<br />
populations are not sustainable.<br />
Recent analyses (Baker 2007; Lees &<br />
Wilcken 2009) and data presented<br />
at the IMP workshop showed that<br />
most of these populations are not<br />
currently being managed at the<br />
numbers of individuals, reliability and<br />
predictability of reproduction and<br />
levels of genetic diversity that would<br />
be required to assure that they can<br />
contribute to species conservation.<br />
Rather than managing for conservation,<br />
the majority of programmes are<br />
managing for “acceptable” levels of<br />
decay and loss, instead of for truly<br />
sustainable, resilient and adaptable<br />
populations that will be available and<br />
suitable to serve conservation needs<br />
in the future. Not surprisingly, some<br />
colleagues within the conservation<br />
and scientific community do not see<br />
the conservation value of intensively<br />
managed ex situ populations.<br />
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42 Intensively Managed <strong>Population</strong>s<br />
WAZA magazine Vol 12/2011<br />
»<br />
Fig. 2<br />
The desired and expected shifts of emphasis among roles. Ex situ facilities have the capacity<br />
and responsibility to focus more of their resources on actions that directly lead to improved<br />
species conservation (arrow A). Moreover, to be able to sustain also exhibit populations<br />
for other purposes, increased management will be needed for those ex situ populations<br />
that will not be easily replaceable (arrow B). As wild environments continue to be<br />
degraded by increasing human activities, it is expected that more species<br />
conservation will require coordinated intensive management of both<br />
ex situ and in situ populations (arrow C).<br />
Zoos can become and be seen as very<br />
powerful forces for species conservation,<br />
not only through the significant<br />
resources that they direct towards<br />
field conservation programmes<br />
(to which members of the WAZA<br />
network contribute more than US$<br />
350 million per year; Gusset & Dick<br />
2011), but also through the direct<br />
conservation roles of the populations<br />
managed within their collections.<br />
Reaching this goal will require<br />
strategic assessment, planning and<br />
action, and this will occur only if<br />
zoos shift their focus from managing<br />
facilities as places with animals<br />
that also do some conservation, to<br />
managing themselves as conservation<br />
organisations that support ex<br />
situ animal populations in order to<br />
reach conservation goals (Fig. 2). The<br />
World Zoo and Aquarium Conservation<br />
Strategy (WAZA 2005) identifies<br />
conservation as the primary purpose<br />
for modern zoological institutions.<br />
However, most zoos are still managed<br />
in ways that demonstrate that<br />
they are focused first on exhibition;<br />
they attend to conservation only<br />
when resources permit or when the<br />
conservation serves the other goals<br />
of the institution.<br />
Changing<br />
the Paradigms<br />
Effecting this shift will not be easy<br />
and will require that zoos change<br />
a number of current practices and<br />
paradigms. At the outset they need<br />
to work more collaboratively with<br />
others in the conservation community,<br />
working together to assess species<br />
for their full range of conservation<br />
needs and developing holistic species<br />
management plans. There are a few<br />
shining examples of collaboration between<br />
Taxon Advisory Groups (TAGs)<br />
of regional zoo associations and the<br />
IUCN/SSC Specialist Groups; this type<br />
of interaction needs to be expanded.<br />
The networks of taxon conservation<br />
experts in the IUCN/SSC Specialist<br />
Groups should be best able to identify<br />
which taxa require intensive management<br />
as part of the species conservation<br />
strategies. However, they are<br />
unlikely to provide that guidance<br />
unless they view the zoo community<br />
as effective partners in conservation.<br />
Achieving that level of confidence in<br />
the role of zoos in species conservation<br />
will require changes in both the<br />
practices and the perception of zoos.<br />
Methods are needed to assess the<br />
need and value for intensive management<br />
and also for prioritising<br />
these taxa; factors to be taken into<br />
account include existing expertise,<br />
capabilities, resources and likelihood<br />
of success. This cannot be accomplished<br />
without reaching outside of<br />
the ex situ community to embrace<br />
other stakeholders, including field<br />
biologists, academics, regional and<br />
global conservation organisations<br />
and interdisciplinary specialists such<br />
as sociologists.
WAZA magazine Vol 12/2011<br />
With clear goals defined by holistic<br />
species management plans, ex situ<br />
programmes will need to be refined<br />
and restructured to maximise success.<br />
The traditional approach of<br />
trying to sustain zoo populations only<br />
through breeding within exhibition<br />
programmes will be sufficient for<br />
only a relatively small number of<br />
species – those that are so popular<br />
that large exhibit populations will<br />
be maintained, that breed readily in<br />
exhibit facilities with little need for<br />
specialised facilities and that are easy<br />
to transport and amenable to periodic<br />
rearrangement of social groups. For<br />
the remaining species, a broader<br />
range of population management<br />
strategies needs to be considered<br />
along a management continuum<br />
(Conway 2011). For some species, this<br />
may mean Global Species <strong>Management</strong><br />
Plans (GSMPs) administered<br />
by WAZA. For others, it may mean<br />
placing breeding individuals into<br />
specialised breeding facilities, while<br />
ensuring that exhibit needs can be<br />
met with non-breeding animals. For<br />
yet others, it may mean exploring<br />
the concept of extractive reserves,<br />
a strategy that the aquarium community<br />
has already made progress in<br />
developing.<br />
Accomplishing the above will require<br />
additional resources and has implications<br />
for how ex situ institutions structure<br />
their financial plans. We will need<br />
to better understand our business<br />
models, questioning assumptions<br />
about what we believe may negatively<br />
impact our ability to manage<br />
species effectively. For example, zoos<br />
often assume that the public wants to<br />
see a huge variety of species and that<br />
if species collections are similar from<br />
zoo to zoo, then attendance will suffer.<br />
We assume that exhibits need to<br />
be large and elaborate to be successful.<br />
These assumptions need to be<br />
tested, as they impact our ability to<br />
develop business plans that expand<br />
our ability to adequately resource<br />
intensive population management in<br />
support of conservation goals.<br />
There are a number of factors that<br />
have contributed to a lack of success<br />
for many IMPs. Common problems<br />
include lack of necessary husbandry<br />
expertise, regulatory obstacles, space<br />
limitations, inadequate founder base<br />
and lack of institutional commitment,<br />
exacerbated by poor communication<br />
among staff and lack of<br />
accountability for those responsible<br />
for implementation of recommendations.<br />
None of these obstacles is insurmountable,<br />
but overcoming them<br />
will require commitment to change.<br />
Discussion among IMP workshop participants<br />
led to the identification of<br />
specific actions needed in areas from<br />
species prioritisation to collection<br />
planning, exploration of new management<br />
approaches and integration<br />
with other conservation efforts and<br />
partners. Putting these recommendations<br />
into action to achieve success<br />
will require concerted efforts by zoo<br />
associations, zoos and individuals. Efforts<br />
are already underway to implement<br />
some of the necessary activities<br />
identified at the IMP workshop. The<br />
scope and urgency of the species conservation<br />
crisis obligates us to move<br />
ahead as quickly as possible.<br />
Intensively Managed <strong>Population</strong>s 43<br />
References<br />
• Baker, A. (2007) Animal ambassadors:<br />
an analysis of the effectiveness<br />
and conservation impact of<br />
ex situ breeding efforts. In: Zoos<br />
in the 21st Century: Catalysts for<br />
Conservation? (ed. by Zimmermann,<br />
A., Hatchwell, M., Dickie,<br />
L. A. & West, C.), pp. 139–154.<br />
Cambridge: Cambridge University<br />
Press.<br />
• Conde, D. A., Flesness, N., Colchero,<br />
F., Jones, O. R. & Scheuerlein,<br />
A. (2011) An emerging role<br />
of zoos to conserve biodiversity.<br />
Science 331: 1390–1391.<br />
• Conway, W. G. (2011) Buying<br />
time for wild animals with zoos.<br />
Zoo Biology 30: 1–8.<br />
• Cook, R. A. (2010) Defining what<br />
it means to save a species – the<br />
species conservation program of<br />
the Wildlife Conservation Society.<br />
In: Proceedings of the 65th WAZA<br />
Annual Conference (ed. by Dick,<br />
G.), pp. 30–31. Gland: WAZA.<br />
• Gusset, M. & Dick, G. (2011)<br />
The global reach of zoos and<br />
aquariums in visitor numbers and<br />
conservation expenditures. Zoo<br />
Biology 30: in press.<br />
• Lees, C. M. & Wilcken, J. (2009)<br />
Sustaining the Ark: the challenges<br />
faced by zoos in maintaining<br />
viable populations. International<br />
Zoo Yearbook 43: 6–18.<br />
• WAZA (2005) Building a Future<br />
for Wildlife: The World Zoo and<br />
Aquarium Conservation Strategy.<br />
Berne: WAZA.
44<br />
© Nicole Gusset-Burgener<br />
Greater flamingo (Phoenicopterus roseus) at Berne Animal Park.<br />
WAZA magazine Vol 12/2011
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WAZA magazine Vol 12/2011